Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins

Genome of human immunodeficiency virus type 1 (HIV-1) is highly heterogeneous. The aim of this work was a phylogenetic study on structural elements of the HIV-1 poly(A) region, in particular polyA and DSE hairpins which compose a core poly(A) site. Methods. The secondary structure of the HIV-1 core...

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Published in:Вiopolymers and Cell
Date:2013
Main Authors: Zarudnaya, M.I., Potyahaylo, A.L., Kolomiets, I.M., Hovorun, D.M.
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Language:English
Published: Інститут молекулярної біології і генетики НАН України 2013
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Online Access:https://nasplib.isofts.kiev.ua/handle/123456789/153248
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Cite this:Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins / M.I. Zarudnaya, A.L. Potyahaylo, I.M. Kolomiets, D.M. Hovorun // Вiopolymers and Cell. — 2013. — Т. 29, №. 6. — С. 454-462. — Бібліогр.: 18 назв. — англ.

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Digital Library of Periodicals of National Academy of Sciences of Ukraine
id nasplib_isofts_kiev_ua-123456789-153248
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spelling Zarudnaya, M.I.
Potyahaylo, A.L.
Kolomiets, I.M.
Hovorun, D.M.
2019-06-13T16:21:49Z
2019-06-13T16:21:49Z
2013
Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins / M.I. Zarudnaya, A.L. Potyahaylo, I.M. Kolomiets, D.M. Hovorun // Вiopolymers and Cell. — 2013. — Т. 29, №. 6. — С. 454-462. — Бібліогр.: 18 назв. — англ.
0233-7657
DOI: http://dx.doi.org/10.7124/bc.00083F
https://nasplib.isofts.kiev.ua/handle/123456789/153248
577.21.5
Genome of human immunodeficiency virus type 1 (HIV-1) is highly heterogeneous. The aim of this work was a phylogenetic study on structural elements of the HIV-1 poly(A) region, in particular polyA and DSE hairpins which compose a core poly(A) site. Methods. The secondary structure of the HIV-1 core poly(A) site has been predicted by the UNAFold program. Results. The structure of the polyA and DSE hairpins has been analysed in 1679 HIV-1 genomes of group M and 18 genomes of simian immunodeficiency virus SIVcpzPtt. We found 244 and 171 different sequences for the HIV-1 polyA and DSE hairpins, respectively. However 70 % of the HIV-1 isolates studied contain one of 7 variants of the polyA hairpin which occur with a frequency 5 % (main variants) and 79 % of the isolates contain one of 7 main variants of the DSE hairpin. We also revealed subtype and country specific mutations in these hairpins. We found that the SIV polyA hairpin most closely resembles that found in HIV-1 genomes of B/C subtypes. Conclusions. The results of our large-scale phylogenetic study support some structural models of the HIV-1 5' UTR, in particular the tertiary interaction between the polyA hairpin and the matrix region in HIV-1 gRNA. Possibly, the DSE hairpin appeared in the course of viral evolution of the HIV-1 group M. An exposure of the U/GU-rich element in the apical loop of DSE hairpin could significantly increase the efficiency of pre-mRNA polyadenylation in this HIV-1 group.
Геном вірусу імунодефіциту людини (ВІЛ-1) надзвичайно гетерогенний. Мета. Провести філогенетичний аналіз структурних елементів області полі(А) ВІЛ-1, зокрема, шпильок поліA і DSE, які складають основний сайт полі(А). Методи. Передбачення вторинної структури основного полі(А)-сайта здійснювали за допомогою програми UNAFold. Результати. Структуру шпильок поліA і DSE проаналізовано для 1679 геномів ВІЛ-1 групи M та 18 геномів вірусу імунодефіциту мавп SIVcpzPtt: у геномах ВІЛ-1 виявлено 244 і 171 різна послідовність шпильок поліA і DSE відповідно. Однак 70 % вивчених геномів містили один із семи варіантів шпильки поліA, які зустрічалися з частотою 5 % (основні варіанти), і 79 % ізолятів вміщують один із семи основних варіантів шпильки DSE. Виявлено також специфічні для певного субтипу або країни мутації зазначених шпильок. Встановлено, що шпилька поліA з геному SIVcpzPtt дуже схожа на таку з геному ВІЛ-1 субтипів B і C. Висновки. Результати наших широкомасштабних досліджень підтримують деякі структурні моделі 5' нетрансльованої ділянки геному ВІЛ-1, зокрема, третинну взаємодію між шпилькою поліA і областю гена матриксного білка. Шпилька DSE, можливо, утворилася у процесі еволюції ВІЛ-1 групи М. Експонування U/GU-збагаченого елемента в апікальній петлі цієї шпильки могло значно підвищити ефективність поліаденілювання про-мРНК у ВІЛ-1 цієї групи.
Геном ВИЧ-1 чрезвычайно гетерогенен. Цель. Провести филогенетический анализ структурных элементов области (поли)А ВИЧ-1, в частности, шпилек полиА и DSE, составляющих основной поли(А)-сайт. Методы. Вторичная структура основного поли(А)-сайта предсказана с помощью программы UNA Fold. Результаты. Структура шпилек полиА и DSE проанализирована в 1679 геномах ВИЧ-1 группы M и 18 геномах вируса иммунодефицита обезьян SIVcpzPtt: в геномах ВИЧ-1 выявлены соответственно 244 и 171 различная последовательность шпилек полиА и DSE. Однако 70 % изученных геномов содержат один из семи вариантов шпильки полиА, встречающихся с частотой 5 % (основные варианты) и 79 % изолятов содержат один из семи основных вариантов шпильки DSE. Обнаружены также варианты шпилек, специфические для определенного субтипа или страны. Выявлено, что шпилька полиА в геноме SIVcpzPtt наиболее близка по структуре таковой в геноме ВИЧ-1 субтипов В и С. Выводы. Результаты наших широкомасштабных исследований свидетельствуют в пользу некоторых структурных моделей 5' нетранслируемой области генома ВИЧ-1, в частности, наличия третичного взаимодействия между шпилькой полиА и участком в гене матриксного белка. Шпилька DSE, возможно, образовалась в процессе эволюции ВИЧ-1 группы М. Экспонирование U/GU- богатого элемента в апикальной петле шпильки DSE могло значи- тельно повысить эффективность полиаденилирования про- мРНК в ВИЧ-1 данной группы.
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Інститут молекулярної біології і генетики НАН України
Вiopolymers and Cell
Structure and Function of Biopolymers
Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins
Філогенетичний аналіз структурних елементів в області полі(А) ВІЛ-1. 1. Шпильки поліA та DSE
Филогенетический анализ структурных элементов в области поли(А) ВИЧ-1. 1. Шпильки полиA и DSE
Article
published earlier
institution Digital Library of Periodicals of National Academy of Sciences of Ukraine
collection DSpace DC
title Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins
spellingShingle Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins
Zarudnaya, M.I.
Potyahaylo, A.L.
Kolomiets, I.M.
Hovorun, D.M.
Structure and Function of Biopolymers
title_short Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins
title_full Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins
title_fullStr Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins
title_full_unstemmed Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins
title_sort phylogenetic study on structural elements of hiv-1 poly(a) region. 1. polya and dse hairpins
author Zarudnaya, M.I.
Potyahaylo, A.L.
Kolomiets, I.M.
Hovorun, D.M.
author_facet Zarudnaya, M.I.
Potyahaylo, A.L.
Kolomiets, I.M.
Hovorun, D.M.
topic Structure and Function of Biopolymers
topic_facet Structure and Function of Biopolymers
publishDate 2013
language English
container_title Вiopolymers and Cell
publisher Інститут молекулярної біології і генетики НАН України
format Article
title_alt Філогенетичний аналіз структурних елементів в області полі(А) ВІЛ-1. 1. Шпильки поліA та DSE
Филогенетический анализ структурных элементов в области поли(А) ВИЧ-1. 1. Шпильки полиA и DSE
description Genome of human immunodeficiency virus type 1 (HIV-1) is highly heterogeneous. The aim of this work was a phylogenetic study on structural elements of the HIV-1 poly(A) region, in particular polyA and DSE hairpins which compose a core poly(A) site. Methods. The secondary structure of the HIV-1 core poly(A) site has been predicted by the UNAFold program. Results. The structure of the polyA and DSE hairpins has been analysed in 1679 HIV-1 genomes of group M and 18 genomes of simian immunodeficiency virus SIVcpzPtt. We found 244 and 171 different sequences for the HIV-1 polyA and DSE hairpins, respectively. However 70 % of the HIV-1 isolates studied contain one of 7 variants of the polyA hairpin which occur with a frequency 5 % (main variants) and 79 % of the isolates contain one of 7 main variants of the DSE hairpin. We also revealed subtype and country specific mutations in these hairpins. We found that the SIV polyA hairpin most closely resembles that found in HIV-1 genomes of B/C subtypes. Conclusions. The results of our large-scale phylogenetic study support some structural models of the HIV-1 5' UTR, in particular the tertiary interaction between the polyA hairpin and the matrix region in HIV-1 gRNA. Possibly, the DSE hairpin appeared in the course of viral evolution of the HIV-1 group M. An exposure of the U/GU-rich element in the apical loop of DSE hairpin could significantly increase the efficiency of pre-mRNA polyadenylation in this HIV-1 group. Геном вірусу імунодефіциту людини (ВІЛ-1) надзвичайно гетерогенний. Мета. Провести філогенетичний аналіз структурних елементів області полі(А) ВІЛ-1, зокрема, шпильок поліA і DSE, які складають основний сайт полі(А). Методи. Передбачення вторинної структури основного полі(А)-сайта здійснювали за допомогою програми UNAFold. Результати. Структуру шпильок поліA і DSE проаналізовано для 1679 геномів ВІЛ-1 групи M та 18 геномів вірусу імунодефіциту мавп SIVcpzPtt: у геномах ВІЛ-1 виявлено 244 і 171 різна послідовність шпильок поліA і DSE відповідно. Однак 70 % вивчених геномів містили один із семи варіантів шпильки поліA, які зустрічалися з частотою 5 % (основні варіанти), і 79 % ізолятів вміщують один із семи основних варіантів шпильки DSE. Виявлено також специфічні для певного субтипу або країни мутації зазначених шпильок. Встановлено, що шпилька поліA з геному SIVcpzPtt дуже схожа на таку з геному ВІЛ-1 субтипів B і C. Висновки. Результати наших широкомасштабних досліджень підтримують деякі структурні моделі 5' нетрансльованої ділянки геному ВІЛ-1, зокрема, третинну взаємодію між шпилькою поліA і областю гена матриксного білка. Шпилька DSE, можливо, утворилася у процесі еволюції ВІЛ-1 групи М. Експонування U/GU-збагаченого елемента в апікальній петлі цієї шпильки могло значно підвищити ефективність поліаденілювання про-мРНК у ВІЛ-1 цієї групи. Геном ВИЧ-1 чрезвычайно гетерогенен. Цель. Провести филогенетический анализ структурных элементов области (поли)А ВИЧ-1, в частности, шпилек полиА и DSE, составляющих основной поли(А)-сайт. Методы. Вторичная структура основного поли(А)-сайта предсказана с помощью программы UNA Fold. Результаты. Структура шпилек полиА и DSE проанализирована в 1679 геномах ВИЧ-1 группы M и 18 геномах вируса иммунодефицита обезьян SIVcpzPtt: в геномах ВИЧ-1 выявлены соответственно 244 и 171 различная последовательность шпилек полиА и DSE. Однако 70 % изученных геномов содержат один из семи вариантов шпильки полиА, встречающихся с частотой 5 % (основные варианты) и 79 % изолятов содержат один из семи основных вариантов шпильки DSE. Обнаружены также варианты шпилек, специфические для определенного субтипа или страны. Выявлено, что шпилька полиА в геноме SIVcpzPtt наиболее близка по структуре таковой в геноме ВИЧ-1 субтипов В и С. Выводы. Результаты наших широкомасштабных исследований свидетельствуют в пользу некоторых структурных моделей 5' нетранслируемой области генома ВИЧ-1, в частности, наличия третичного взаимодействия между шпилькой полиА и участком в гене матриксного белка. Шпилька DSE, возможно, образовалась в процессе эволюции ВИЧ-1 группы М. Экспонирование U/GU- богатого элемента в апикальной петле шпильки DSE могло значи- тельно повысить эффективность полиаденилирования про- мРНК в ВИЧ-1 данной группы.
issn 0233-7657
url https://nasplib.isofts.kiev.ua/handle/123456789/153248
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fulltext STRUCTURE AND FUNCTION OF BIOPOLYMERS UDC 577.21.5 Phylogenetic study on structural elements of HIV-1 poly(A) region. 1. PolyA and DSE hairpins M. I. Zarudnaya, A. L. Potyahaylo, I. M. Kolomiets, D. M. Hovorun Institute of Molecular Biology and Genetics, NAS of Ukraine 150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03680 m.i.zarudna@imbg.org.ua Genome of human immunodeficiency virus type 1 (HIV-1) is highly heterogeneous. Aim. A phylogenetic study on structural elements of the HIV-1 poly(A) region, in particular polyA and DSE hairpins which compose a core poly(A) site. Methods. The secondary structure of the HIV-1 core poly(A) site has been pre- dicted by the UNAFold program. Results. The structure of the polyA and DSE hairpins has been analysed in 1679 HIV-1 genomes of group M and 18 genomes of simian immunodeficiency virus SIVcpzPtt. We found 244 and 171 different sequences for the HIV-1 polyA and DSE hairpins, respectively. However 70 % of the HIV-1 isolates studied contain one of 7 variants of the polyA hairpin which occur with a frequency �5 % (main variants) and 79 % of the isolates contain one of 7 main variants of the DSE hairpin. We also revealed subtype and country specific mutations in these hairpins. We found that the SIV polyA hairpin most closely resembles that found in HIV-1 genomes of B/C subtypes. Conclusions. The results of our large-scale phylogenetic study support some structural models of the HIV-1 5' UTR, in particular the tertiary interaction between the polyA hairpin and the matrix region in HIV-1 gRNA. Possibly, the DSE hairpin appeared in the course of viral evolution of the HIV-1 group M. An exposure of the U/GU-rich element in the apical loop of DSE hairpin could significantly increase the efficiency of pre-mRNA polyadenylation in this HIV-1 group. Keywords: HIV-1, SIVcpzPtt, poly(A) region, secondary structure, polyA hairpin, DSE hairpin. Introduction. Polyadenylation of the pre-mRNAs in mammals and their viruses depends on at least two se- quence elements: the poly(A) signal (most often the AAUAAA hexamer) and the U/GU-rich downstream sequence element (DSE). These elements compose the core poly(A) site. Multiple protein factors assemble on- to this site, in particular, the cleavage and polyadeny- lation specificity factor (CPSF) binds to the AAUAAA hexamer and the cleavage stimulation factor (CstF) binds to the U/GU-rich DSE [1, 2]. The efficiency of po- lyadenylation process can be modulated by upstream se- quence elements (USEs) or/and auxiliary downstream sequence elements (AuxDSEs) [3]. In the HIV-1 retro- virus, the identical sequences encompassing AAUAAA and DSE are present at both the 5' and 3' ends of the HIV-1 pre-mRNA and a strict regulation is needed to re- press the premature polyadenylation at the 5' end of the transcript and stimulate the reaction at the 3' end. In par- ticular, usage of the 3' poly(A) site is promoted by the USEs that are present exclusively at the 3' end of the transcript [4]. In HIV-1 pre-mRNA, the AAUAAA hexamer is partly occluded by base pairing in the upper part of the polyA hairpin [5], the stability of which is delicately ba- lanced to allow the regulation of polyadenylation reac- tion at the both ends [6]. Two putative DSEs, UGUGU and GUUGUGU, are located 6 and 19 nt downstream of the cleavage site, respectively. Recently we have first presented a structural model for the core poly(A) site at the 3' end of the HIV-1 pre-mRNA [7] (Fig 1). The tracts interacting with the polyadenylation factors as well as other functionally important elements are indicated in this figure. The other elements are functional at the 5' end of HIV-1 genomic RNA (gRNA), inasmuch as they 454 ISSN 0233–7657. Biopolymers and Cell. 2013. Vol. 29. N 6. P. 454–462 doi: 10.7124/bc.00083F � Institute of Molecular Biology and Genetics, NAS of Ukraine, 2013 455 PHYLOGENETIC STUDY ON STRUCTURAL ELEMENTS OF HIV-1 POLY(A) REGION are located in the long terminal repeats of proviral DNA they are also duplicated at the 3' end of the transcript. HIV-1 genome is highly heterogeneous. The aim of this work was a large-scale phylogenetic study on the structural elements of the HIV-1 poly(A) region. First we investigated how mutations in the polyA and DSE hair- pins affect their secondary structure and also compared the structure of these elements in HIV-1 pre-mRNAs and pre-mRNAs of simian immunodeficiency virus of chimpanzee Pan troglodytes troglodytes (SIVcpzPtt). Materials and methods. The sequences encompas- sing the complete poly(A) region in HIV-1 and SIV ge- nomes have been extracted from the Entrez Nucleotide database of NCBI. We have examined all HIV-1 geno- mic sequences presented in this database by the end of 2010 and all corresponding genomic sequences from SIVcpzPtt and SIVgor (gorilla) presented by the end of 2012. The secondary structure of the poly(A) site has been predicted by the UNAFold program [11]. The ba- se changes in sequences of HIV-1 and SIV pre-mRNAs were determined as compared to RefSec (the HXB2 iso- late, GenBank accession number K03455). Nucleotide numbering starts with 1 at the first nucleotide of each in- dividual structural element. Results and discussion. PolyA hairpin. We have ana- lysed the structure of elements of the HIV-1 core poly(A) site for 1679 HIV-1 pre-mRNAs of group M (isolated from 997 patients) and found 244 different sequences for the polyA hairpin. These sequences contained up to ele- ven base changes in comparison with the RefSec. The polyA hairpins with the combination of base changes oc- curring with a frequency � 5 % (the main variants, pA1– pA7) are shown in Fig. 2. Their distribution by subtypes A–C, and CRF01_AE, comprising large sub pools, is gi- ven in Table 1. The total data on other subtypes and CRFs comprising small subpools are listed in the last column. All main variants of the polyA hairpin have identi- cal upper part with a partly occluded AAUAAA hexa- mer, while their stems contain different small defects (bulges and internal loops). As seen in Table 1, some po- lyA hairpin variants, for example pA1 (without muta- tions) and pA2 (with the C39U base substitution) occur in HIV-1 isolates of several subtypes with different frequencies, while other variants occur mainly in HIV- 1 isolates of certain subtypes. In HIV-1 isolates of sub- types D, F and G, the variants pA1 and pA2 are the most frequent. It is of interest to note that none of the base changes occurring in the main variants of polyA hair- pin of subtype C isolates (pA4 and pA7) was found in the main variants of CRF01_AE (pA5 and pA6). Depending on the subtype, 52–84 % of HIV-1 isola- tes contain one of main variants of the polyA hairpin (Table 1). However, within a certain subtype their oc- currence may be country specific. For example, the po- lyA hairpin with the double mutation U38C + C39U (pA4) occurs often in HIV-1 isolates of subtype C from the African countries: Mozambique (35 %), South Af- rica (47 %), Tanzania (54 %), and Zambia (72 %) and rarely in Indian HIV-1 isolates (3 %). On the contrary, the variant with the four base changes (pA7) occurs fre- quently (55 %) in subtype C isolates from India and ra- rely or is absent in the African countries. Some polyA hairpins occurring with a frequency < 5 % in the HIV-1 isolates studied, though not presented in Table 1, are ra- ther frequent in certain countries, for example, the hair- pin with base changes C36A + U37C + U43C (pA8, Fig. 2) was found in 10 % of subtype A isolates from Tanzania. In general 70 % of all HIV-1 isolates studied have one of the 7 main variants of the polyA hairpin. What are the peculiarities of the polyA hairpin formed in the rest of HIV-1 isolates? Table 2 is given to illust- rate this issue. It shows the base changes in the polyA hairpin for 26 HIV-1 isolates of subtype C from Mozam- bique, which comprise half of the whole pool of these isolates. As many as 54 % of HIV-1 isolates presented A-U A-U C-G U-A C-G U C-G G-C A-U A-U C U-A U-A C-G G-U U-A C-G A-U C-G C-G U-A G-C C-G C-G G-U U-AU G U U C C U G U G U U G U A U A G A C U C G UC 1 2 3 9650 9600 Fig. 1. The 3' core poly(A) site of HIV-1 HXB2 pre-mRNA (RefSec). Nucleotide positions are numbered as in the HXB2 genome. The AAU AAA hexamer and the U/GU-rich signals are shadowed. The motifs which are functional at the 5' end of HIV-1 genome: 1 – involved in the long distance interaction with the matrix coding region [8]; 2 – the 5' strand of U5-AUG duplex [9]; 3 – a primer activation signal (PAS) regulating the initiation of reverse transcription [10] in Table 2 have one of the main polyA hairpin variants such as pA4 (42 %), pA2 (8 %) and pA7 (4 %). The polyA hairpins in the rest of isolates can be considered as these three main variants with one or two base chan- ges which occur with different frequencies in the HIV- 1 isolates studied. For example, A32G (GenBank acc. no. AM076852) occurs with a frequency below the error of sequencing and submission of HIV-1 genomic sequence into Gen Bank (0.5 % [12]), while A44G (AM076846) is very frequent in HIV-1 isolates of subtype CRF01_AE but is random in isolates of subtype C. Precisely rare and ran- dom base changes lead to a great variety in sequences of the polyA hairpin. The rare and random mutations pre- sented in Table 2 did not affect greatly the overall struc- ture of the polyA hairpin, except for G31A (AM076874). This base change occurs singly or in the combination with different mutations with a frequency of 2.1 % in the HIV-1 isolates studied. In most cases, it results in two alternative conformations of the hairpin with the 456 ZARUDNAYA M. I. ET AL. pA2 -18.5 pA3 -16.5 pA4 -18.5 pA5 -18.1 pA6 -18.1 pA7 -20.6 pA8 A-U A-U C-G U-A C-G G-C A-U A C U-A U-A C-G G-C U-A C-G A-U C C-G U A U A G A C U C G UC U A C G pA9 -14.8 -14.9 A-U A-U C-G U-A C-G G-C A-U A-U U-G U-A C-G G-C U-A C-G A-U C C-G U A U A G A C U C G UC U A C G pA10 -18.8 G, kcal/molÄ pA1 1 10 20 30 40 -18.5 A-U A-U C-G U-A C-G U C-G G-C A-U A-U C U-A U-A C-G G-U U-A C-G A-U C C-G U A U A G A C U C G UC A-U A-U C-G U-A C-G U C-G G-C A-U C A U-A U-A C-G G-U U-A C-G A-U C C-G U A U A G A C U C G UC A A-U A-U C-G U-A C-G U C-G G-C A-U C A-U U-A U-A C-G G-U U-A C-G A-U C C-G U A U A G A C U C G UC A-U A-U C-G U-A C-G U C-G G-C A-U A-U A A U-A U-A C-G G U U G C-G A-U C C-G U A U A G A C U C G UC A-U A-U C-G U-A C-G U C-G G-C A-U A-U A G U-A U-A C-G G U U G C-G A-U C C-G U A U A G A C U C G UC A-U A-U C-G U-A C-G U C-G G-C A-U C A-U U-G U-A C-G G-C U-A C-G A-U C C-G U A U A G A C U C G UC A-U A-U C-G U-A C-G U C-G G-C U A-U A-U U-A U-A C-G G-U U-A C-G A-U C C-G U A U A G A C U C G UC A A A G U C A-U A-U C-G U-A C-G U C-G G-C A-U C A-U U-G U-A C-G G-C U-A C-G A-U C C-G U C U U C A C C U G-U U-A U-A C-G G-U C-G G-C A-U C A-U U-G U-A C-G G-C U-A C-G A-U C C-G U CU C A A U A A A Fig. 2. Optimal structures of polyA hairpin variants in HIV-1 and SIVcpzPtt pre-mRNAs. The base changes as compared to RefSec are squared, insertions and deletions are indicated by triangle and spot, respectively. The AAUAAA hexamer is shadowed. pA1–pA7 – main variants of the polyA hairpin in HIV-1 isolates of group M; pA8 – rather frequent variant in subtype A isolates from Tanzania; pA9 – variant with the G31A base change; pA10 – polyA hairpin variant in SIVcpzPtt isolates Variant Base changes Subtype A B C CRF01_AE Others Number of HIV-1 isolates (number of patients) 141 (122) 645 (258) 291 (234) 162 (61) 440 (322) pA1 No 17 50 2 0 42 pA2 C39U 32 27 8 0 10 pA3 U38C + C39A 0 6 1 0 0.4 pA4 U38C + C39U 3 1 40 0 8 pA5 10_11ins A + C39A + A44G 0 0.1 0 46 1 pA6 10_11ins A + C39G + A44G 0 0 0 6 0 pA7 U38C + C39U + A40G + U43C 0 0.1 15 0 2 Total – 52 84 67 52 63 Table 1 Occurrence of polyA hairpin variants in HIV-1 isolates of different subtypes (%) same free energy and complete exposure of the AAUA AA hexamer in one of these conformations (for examp- le, see pA9 in Fig. 2). As seen in Table 2, the double mutation U38C + + C39U (both as the pA4 variant and in combination with other base changes) is prevailing among the HIV- 1 isolates from Mozambique (77 %). The availability of a certain motif containing one or several frequent base changes in combination with rare and/or random muta- tions is also characteristic of the polyA hairpins in HIV- 1 isolates of other subtypes. It is also a peculiarity of other structural elements in the HIV-1 polyA region. 457 PHYLOGENETIC STUDY ON STRUCTURAL ELEMENTS OF HIV-1 POLY(A) REGION Accession number Patient Base changes in polyA hairpin PolyA hairpin Position 7 10 31 32 36 37 38 39 40 43 44 AM076840 PG174 A10G U38A C39U AM076842 PG174 A10G U38A C39U AM076844 PG81 U38C C39U pA4 AM076846 PG56 U38C C39U A44G AM076848 PG5 U38C C39U pA4 AM076850 PG5 U38C C39U pA4 AM076852 PG6 A32G C39U AM076854 PG184 U38C C39U pA4 AM076856 PG196 U38C C39U pA4 AM076858 PG182 U38C C39U A40G AM076860 PG182 U38C C39U A40G AM076862 PG188 U38C C39U pA4 AM076864 PG189 C36U U38C C39U A40G U43C AM076866 PG203 U38C C39U A40G AM076868 PG215 C39U pA2 AM076870 PG224 U38C C39U pA4 AM076872 PG227 U38C C39U A40G U43C pA7 AM076874 PG227 G31A U38C C39U A40G U43C AM076876 PG227 U7C C36U U38C C39U A40G U43C AM076878 PG230 C36A U37C C39U AM076880 PG231 U38C C39U pA4 AM076882 PG177 C39U pA2 AM076884 PG178 U38C C39U pA4 AM076886 PG217 U38C C39U pA4 AM076888 PG218 C36U U38C C39U AM076891 PG36 U38C C39U pA4 Table 2 Base changes in polyA hairpin of HIV-1 subtype C isolates from Mozambique In general the base changes which led to significant alterations in the polyA hairpin structure occurred only in 4 % of all HIV-1 genomes studied. The structures of the polyA region in the HIV-1 isolates studied are presen- ted in our database CESSHIV-1 which is currently avai- lable online at http://www.cesshiv1.org. Base change fre- quency at each position of the polyA hairpin is presen- ted in Suppl. information (Table S1). Rather frequent mu- tations in this element are an insertion between positions 10, 11 and base changes at positions 37–40, 43, and 44. HIV-1 gRNA contains several strong binding sites for multifunctional virion infectivity factor (Vif) inclu- ding the polyA hairpin [13]. In particular, Vif-RNA interaction is important for viral particle assembly. Vif specifically binds to the stem of polyA hairpin, however structural and sequence determinants of this binding 458 ZARUDNAYA M. I. ET AL. 5 10 15 20 25 30 0 20 40 60 80 100 120 1220 1240 5 10 15 20 25 30 0 10 20 30 N u m b er ÄG kcal/mol A N u m b er ÄG kcal/mol B Fig. 3. Free energy distribution of HIV-1 polyA hairpin variants: A – all 1863 polyA hairpins; B – 286 HIV-1 polyA hairpins with different sequences (see Section PolyA hairpin) are not defined. Various defects in the stem of polyA hairpin (Fig. 2) can modulate its binding to Vif. Base changes in the AAUAAA hexamer and the neighbouring GCUUGCC tract occur with a frequency below the error level, except for a position 28 in the po- lyA hairpin at which mutations occur with a frequency of 0.7 %. We have also shown high conservation of the sequence GGCAAGC in the matrix region of HIV-1 gRNA for a large pool of HIV-1 isolates. Thus, our data support a statement about the long distance interaction between the GCUUGCC and GGCAAGC sequences important for the tertiary structure of the 5' untranslated region of HIV-1 gRNA [8]. As mentioned in Introduction, a balanced stability of the polyA hairpin is crucial for HIV-1 replication [6, 14]. Both destabilization and stabilization of the wild type hairpin inhibits polyadenylation of HIV-1 pre- mRNA at the 3' end of the transcript. Stabilization of this hairpin by 10.4 kcal/mol blocked the access of po- lyadenylation factors to the hexamer and led to comp- lete loss of polyadenylation at the 3' end of HIV-1 pre- mRNA [6, 14]. Destabilization by 8.5 kcal/mol increa- sed the efficiency of premature polyadenylation at the 5' end of HIV-1 transcript from 5–10 % to 30–40 % [14], that affects less severely polyadenylation at the 3' end than stabilization of the polyA hairpin. It was 459 PHYLOGENETIC STUDY ON STRUCTURAL ELEMENTS OF HIV-1 POLY(A) REGION G, kcal/molÄ 1 1 10 10 20 20 U U G G U U U G C-G U-A G-C C-G C-G G-U G U-A A U C C U U U G G U U U G C-G U-A C-G C-G G-U G U-A A C U C U A C U U G A U U U G C-G U-A G-C C-G C-G G-U G U-A A U C C U U U G U U U U G C-G U-A G-C C-G C-G G-U G U-A A U C C U G U U U G A U-G C-G U-A G-C C-G C-G G-U G U-A A U C C U C U C U A C G U U U G A U-G C-G U-A C-G C-G G-U G U-A A C U C U A C U U G G U U C-G U-A C-G C-G G-U G U-A A U U A G U U U G C-G U-A G-C C-G C-G G-U G U-A A U C C U DSE1 DSE2 DSE3 DSE4 DSE5 U A A G U U U C C-G U-A G-C C-G C-G G-U U-A U G-U C U C C U A U A U U C-G U C-G U-A C-G C-G G-U U-A U G-U C C U C U A C U A A G U U U C C-G U-A C-G C-G G-U U-A U G-U C C U C U A U DSE6 DSE7 DSE8 DSE 1SIV DSE 2SIV DSE 3SIV -5.4 -2.2 -5.4 -5.4 -5.4 -6.5 -3.3 -2.4 -4.0 -2.6 -6.5 Fig. 4. Optimal structures of DSE hairpin variants in HIV-1 and SIVcpzPtt pre-mRNAs. The base changes as compared to RefSec are squared, de- letions are indicated by spot. The U/GU-rich DSE signal is shadowed. DSE1–DSE7 – main variants of the DSE hairpin in HIV-1 isolates of group M (for DSE2 a suboptimal structure with free energy difference of –0.9 kcal/mol is shown); DSE8 – frequent variant in subtype D isolates; DSE SIV 1–DSE SIV 3 – DSE-like hairpin variants in SIVcpzPtt isolates Variant Base changes Subtype A B C CRF01_AE Others Number of HIV-1 isolates (number of patients) 141 (122) 645 (258) 291 (234) 162 (61) 440 (322) DSE1 RS 30.5 76.0 65.3 0 58.6 DSE2 G6A 3.5 7.3 6.5 0 7.7 DSE3 G10A 0 2.2 5.5 0 1.8 DSE4 G15A 36.9 0.5 1.0 0 3.9 DSE5 G15U 7.1 0.1 0.7 0 3.6 DSE6 U12G + G13U + G15A + U16G 0 0 0 43.8 0.9 DSE7 G6A + U12G + G13U + G15A + U16G 0 0 0 13.6 0 Total – 78 86 79 57 76 Table 3 Occurrence of DSE hairpin variants in HIV-1 isolates of different subtypes (%) shown by the method of virus evolution that HIV-1 mu- tants with stabilized or destabilized polyA hairpin have improved their replication capacity via drifting towards a hairpin of thermodynamic stability that is close to the value of the wild type hairpin [15]. Free energy distribution of the HIV-1 polyA hairpins is presented in Fig. 3, A. Here we have analysed the HIV- 1 genomes which contain both the complete poly(A) re- gion (see Materials and methods) and incomplete regions encompassing a polyA hairpin sequence (see CESSHIV- 1 database). In sum we have analyzed 1863 genomes (from 1072 patients) which contain 286 different sequen- ces of the polyA hairpin. For two patients with multiple identical sequences of the polyA hairpin, we considered for analysis only one intrapatient sequence. The major peak in Fig. 3, A, corresponds to the HIV- 1 isolates containing the polyA hairpins with free ener- gy (dG) of –18.5 kcal/mol. The main variants of the po- lyA hairpin pA1, pA2 and pA4 make a major contribu- tion to this peak (92 %), while other main variants cont- ribute to minor peaks at –16.5, –18.1 and –20.6 kcal/mol. The minor peak at –12.8 kcal/mol corresponds mostly to the polyA hairpins with the base change G31A and double mutation G31A + C39U. Free energy distribution of the 286 HIV-1 polyA hair- pins with different sequences is shown in Fig. 3, B. In ge- neral both distributions are similar. The main peak in Fig. 3, B, also corresponds to –18.5 kcal/mol. A maximal num- ber of different sequences of the polyA hairpin (29 ones) contribute to this peak. Both distributions are skewed, in particular the number of HIV-1 isolates with the polyA hairpins with dG > –18.5 kcal/mol (26.9 %) significantly exceeds that with dG < –18.5 kcal/mol (6.5 %). Free energy distributions of the HIV-1 polyA hair- pins for different subtypes (A, B, C, D, G, CRF01_AE and CRF02_AG) are similar to those presented in Fig. 3, A. All distributions are skewed and have the maxi- mum at –18.5 kcal/mol, except that the plot for CRF01_ AE has a maximum at –18.1 kcal/mol. Thus, a free ener- gy of the polyA hairpin lies within the range of –10.9 � � –20.9 kcal/mol in most HIV-1 isolates (98.5 %), and the polyA hairpin with dG of –18.5 kcal/mol is found in 66.6 % isolates. To gain insight into the evolution of frequent muta- tions in HIV-1 polyA hairpin we studied a structure of the core poly(A) site in 18 isolates of SIVcpzPtt that is an ancestor of HIV-1 group M [16]. Similarity of the po- lyA hairpin in SIVcpzPtt and HIV-1 was first reported by Berkhout et al. [5]. The SIV polyA hairpin presented in their article possesses the upper part identical to that in HIV-1 HXB2 genome and a stem with two bulges 0� � 2 and 0 � 1. In our study we found 14 different sequ- ences of the SIV polyA hairpin, including the sequences identical to the HIV-1 polyA hairpin variants pA1, pA2 and pA4. All SIV isolates have the polyA hairpin with the common upper part, except for three isolates in which the apical loop is elongated by 2 nucleotides (nt) thus exposing 5 nt instead of 4 nt of the AAUAAA hexamer. The combination of base changes 35_36insA + + C39del + A40G + U43C can be considered as a fre- quent motif of the SIV polyA hairpin (Supplementary information, Table S2). Three SIV isolates have the po- lyA hairpin containing exclusively this motif (pA10, Fig. 2). The double mutation 35_36insA + C39del was found in three HIV-1 polyA hairpins (two isolates of subtype C and one of subtype B) and A40G + U43C is a constituent of the combination of base changes in the HIV-1 polyA variant pA7 specific for subtype C isolates. DSE hairpin. The variants of HIV-1 DSE hairpin with combinations of base changes occurring with a frequency � 5 % (the main variants, DSE1-DSE7) are shown in Fig. 4. Their distribution by subtype is given in Table 3. The variants DSE1-DSE3 are found in HIV-1 isolates of different subtypes, while the variants DSE4– DSE7 occur predominantly in HIV-1 isolates of certain subtype. HIV-1 isolates of subtypes D, F and G com- monly have the DSE hairpin without mutations (DSE1), except that the variant with the base changes G6A + + U16del + G17del (DSE8, Fig. 4) occurs rather fre- quently in HIV-1 isolates of subtype D (19 %). About 80 % of the HIV-1 isolates studied have one of the main DSE hairpin variants. The apical loop is the most variable region of the DSE hairpin (Supplementary information, Table S3). In the U/GU-rich tract, frequent base changes occur at positions 12, 13, 15 and 16. The combination of these four base changes, which is specific for CRF01_AE, does not impair DSE signal (DSE6, Fig. 4). According to our description of the mammalian DSE region [17], it is composed of certain U/GU-rich pentamers (in par- ticular the GUUGU, UGUGU or GUGUU tracts) which are located at different distances from each other. All the- 460 ZARUDNAYA M. I. ET AL. se pentamers are found in the apical loop of the main va- riants of the DSE hairpin as single or overlapping tracts. In DSE5, the GUUGU pentamer overlaps the UGUUU tract which is a U-rich (URE) DSE signal of the type «a four out of five base URE» [18]. In some HIV-1 isolates of CRF01_AE, the mutations at positions 12 and/or 13 impair DSE signal by preventing a complete exposure of the U/GU-rich tract, which can decrease an efficiency of the polyadenylation process. It concerns mainly the group of 46 HIV-1 isolates from 3 patients, which pos- sess the DSE hairpin with a combination of base chan- ges G6A + C8U + U12del + G15C + U16A + 17G18. The sequences of both strands of the DSE hairpin stem are well conserved. The rather frequent base chan- ge G6A destabilizes the hairpin and leads to partial oc- clusion of the U/GU-rich tract in the optimal structure; however this tract is completely exposed in a the subop- timal structure with close free energy (DSE2, Fig. 4). Rare mutations (4 %) occur at position 17 (deletion and G17A base change) and between positions 17 and 18 (insertion). The deletion occurs in 39 % of HIV-1 isola- tes of subtype D and does not affect DSE signal exposu- re (DSE8, Fig. 4). The insertion 17G18 in combina- tions with some base changes impairs DSE signal ex- posure, mainly in the above mentioned group of 46 iso- lates of CRF01_AE. The 5' strand of the DSE hairpin together with two neighboring residues (tract 2 in Fig. 1) correspond to the 5' strand of the U5-AUG duplex formed at the 5' end of HIV-1 gRNA. The mutation G6A in the DSE hairpin corresponds to G9651A in HXB2 genome resulting in a G-U to A-U base pair substitution in the duplex. We have shown that the 3' strand of this duplex is also well con- served in a large pool of HIV-1 isolates, which supports the formation of the U5-AUG duplex. The conservation of tract 3 encompassing PAS signal supports its func- tional importance, including tRNA3 Lys-PAS interaction. In the SIV isolates studied, we have not found a hair- pin similar to the HIV-1 DSE hairpin as distinct from the polyA hairpin occurred in both HIV-1 and SIV. How- ever a hairpin with the bottom duplex like in the HIV-1 DSE hairpin (frequently with an additional base pair G-U) was found in almost all SIV isolates (DSESIV1- DSESIV3, Fig. 4). The main difference between the HIV-1 DSE hairpin and its SIV analogue is the absence of the U/GU-rich tract in the DSESIV apical loop. Only one SIV hairpin has such tract but not completely ex- posed (DSESIV2, Fig. 4). Probably, SIV isolates use UGUGU signal just downstream of the polyA hairpin (Fig. 1) that is partly occluded. The strains of HIV-1 are classified into four groups: M, N, O and P which are of chimpanzee or gorilla ori- gin [16]. We have not found any DSE hairpin exposing the U/GU-rich tract in either HIV-1 groups N, O and P (36 isolates) or SIV from gorilla (5 isolates). We hy- pothesize that the U/GU-rich tract exposed in the apical loop of DSE hairpin has been acquired in HIV-1 group M in the course of evolution. At present it is poorly un- derstood why only group M, but not other HIV-1 groups, resulted in a global pandemic [16]. An effective DSE may be one of the features that makes group M much more prevalent than groups N, O and P. Ì. ². Çàðóäíà, À. Ë. Ïîòÿãàéëî, I. M. Êîëî쳺öü, Ä. M. Ãîâîðóí Ô³ëîãåíåòè÷íèé àíàë³ç ñòðóêòóðíèõ åëåìåíò³â â îáëàñò³ ïîë³(À) ²Ë-1. 1. Øïèëüêè ïîë³A òà DSE Ðåçþìå Ãåíîì â³ðóñó ³ìóíîäåô³öèòó ëþäèíè (²Ë-1) íàäçâè÷àéíî ãåòåðî- ãåííèé. Ìåòà. Ïðîâåñòè ô³ëîãåíåòè÷íèé àíàë³ç ñòðóêòóðíèõ åëå- ìåíò³â îáëàñò³ ïîë³(À) ²Ë-1, çîêðåìà, øïèëüîê ïîë³A ³ DSE, ÿê³ ñêëàäàþòü îñíîâíèé ñàéò ïîë³(À). Ìåòîäè. Ïåðåäáà÷åííÿ âòî- ðèííî¿ ñòðóêòóðè îñíîâíîãî ïîë³(À)-ñàéòà çä³éñíþâàëè çà äîïî- ìîãîþ ïðîãðàìè UNAFold. Ðåçóëüòàòè. Ñòðóêòóðó øïèëüîê ïî- ë³A ³ DSE ïðîàíàë³çîâàíî äëÿ 1679 ãåíîì³â ²Ë-1 ãðóïè M òà 18 ãå- íîì³â â³ðóñó ³ìóíîäåô³öèòó ìàâï SIVcpzPtt: ó ãåíîìàõ ²Ë-1 âèÿâ- ëåíî 244 ³ 171 ð³çíà ïîñë³äîâí³ñòü øïèëüîê ïîë³A ³ DSE â³äïîâ³äíî. Îäíàê 70 % âèâ÷åíèõ ãåíîì³â ì³ñòèëè îäèí ³ç ñåìè âàð³àíò³â øïè- ëüêè ïîë³A, ÿê³ çóñòð³÷àëèñÿ ç ÷àñòîòîþ �5 % (îñíîâí³ âàð³àíòè), ³ 79 % ³çîëÿò³â ì³ñòÿòü îäèí ³ç ñåìè îñíîâíèõ âàð³àíò³â øïèëüêè DSE. Âèÿâëåíî òàêîæ ñïåöèô³÷í³ äëÿ ïåâíîãî ñóáòèïó àáî êðà¿íè ìóòàö³¿ çàçíà÷åíèõ øïèëüîê. Âñòàíîâëåíî, ùî øïèëüêà ïîë³A ç ãå- íîìó SIVcpzPtt äóæå ñõîæà íà òàêó ç ãåíîìó ²Ë-1 ñóáòèï³â B ³ C. Âèñíîâêè. Ðåçóëüòàòè íàøèõ øèðîêîìàñøòàáíèõ äîñë³äæåíü ï³äòðèìóþòü äåÿê³ ñòðóêòóðí³ ìîäåë³ 5' íåòðàíñëüîâàíî¿ ä³ëÿí- êè ãåíîìó ²Ë-1, çîêðåìà, òðåòèííó âçàºìîä³þ ì³æ øïèëüêîþ ïî- ë³A ³ îáëàñòþ ãåíà ìàòðèêñíîãî á³ëêà. Øïèëüêà DSE, ìîæëèâî, óòâîðèëàñÿ ó ïðîöåñ³ åâîëþö³¿ ²Ë-1 ãðóïè Ì. Åêñïîíóâàííÿ U/ GU-çáàãà÷åíîãî åëåìåíòà â àï³êàëüí³é ïåòë³ ö³º¿ øïèëüêè ìîãëî çíà÷íî ï³äâèùèòè åôåêòèâí³ñòü ïîë³àäåí³ëþâàííÿ ïðî-ìÐÍÊ ó ²Ë-1 ö³º¿ ãðóïè. Êëþ÷îâ³ ñëîâà: ²Ë-1, SIVcpzPtt, îáëàñòü ïîë³(À), âòîðèííà ñòðóêòóðà, øïèëüêà ïîë³À, øïèëüêà DSE. Ì. È. Çàðóäíàÿ, À. Ë. Ïîòÿãàéëî, È. Í. Êîëîìèåö, Ä. Í. Ãîâîðóí Ôèëîãåíåòè÷åñêèé àíàëèç ñòðóêòóðíûõ ýëåìåíòîâ â îáëàñòè ïîëè(À) ÂÈ×-1. 1. Øïèëüêè ïîëèA è DSE Ðåçþìå Ãåíîì ÂÈ×-1 ÷ðåçâû÷àéíî ãåòåðîãåíåí. Öåëü. Ïðîâåñòè ôèëîãå- íåòè÷åñêèé àíàëèç ñòðóêòóðíûõ ýëåìåíòîâ îáëàñòè (ïîëè)À ÂÈ×- 461 PHYLOGENETIC STUDY ON STRUCTURAL ELEMENTS OF HIV-1 POLY(A) REGION 462 ZARUDNAYA M. I. ET AL. 1, â ÷àñòíîñòè, øïèëåê ïîëèÀ è DSE, ñîñòàâëÿþùèõ îñíîâíîé ïî- ëè(À)-ñàéò. Ìåòîäû. Âòîðè÷íàÿ ñòðóêòóðà îñíîâíîãî ïîëè(À)- ñàéòà ïðåäñêàçàíà ñ ïîìîùüþ ïðîãðàììû UNA Fold. Ðåçóëüòà- òû. Ñòðóêòóðà øïèëåê ïîëèÀ è DSE ïðîàíàëèçèðîâàíà â 1679 ãå- íîìàõ ÂÈ×-1 ãðóïïû M è 18 ãåíîìàõ âèðóñà èììóíîäåôèöèòà îáå- çüÿí SIVcpzPtt: â ãåíîìàõ ÂÈ×-1 âûÿâëåíû ñîîòâåòñòâåííî 244 è 171 ðàçëè÷íàÿ ïîñëåäîâàòåëüíîñòü øïèëåê ïîëèÀ è DSE. Îäíàêî 70 % èçó÷åííûõ ãåíîìîâ ñîäåðæàò îäèí èç ñåìè âàðèàíòîâ øïèëü- êè ïîëèÀ, âñòðå÷àþùèõñÿ ñ ÷àñòîòîé �5 % (îñíîâíûå âàðèàíòû) è 79 % èçîëÿòîâ ñîäåðæàò îäèí èç ñåìè îñíîâíûõ âàðèàíòîâ øïèëüêè DSE. Îáíàðóæåíû òàêæå âàðèàíòû øïèëåê, ñïåöèôè- ÷åñêèå äëÿ îïðåäåëåííîãî ñóáòèïà èëè ñòðàíû. Âûÿâëåíî, ÷òî øïèëüêà ïîëèÀ â ãåíîìå SIVcpzPtt íàèáîëåå áëèçêà ïî ñòðóêòóðå òàêîâîé â ãåíîìå ÂÈ×-1 ñóáòèïîâ  è Ñ. Âûâîäû. Ðåçóëüòàòû íà- øèõ øèðîêîìàñøòàáíûõ èññëåäîâàíèé ñâèäåòåëüñòâóþò â ïîëüçó íåêîòîðûõ ñòðóêòóðíûõ ìîäåëåé 5' íåòðàíñëèðóåìîé îáëàñòè ãåíîìà ÂÈ×-1, â ÷àñòíîñòè, íàëè÷èÿ òðåòè÷íîãî âçàèìîäåéñò- âèÿ ìåæäó øïèëüêîé ïîëèÀ è ó÷àñòêîì â ãåíå ìàòðèêñíîãî áåëêà. 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