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Research Article | Host-Microbe Biology

Low Postseroconversion CD4+ T-cell Level Is Associated with Faster Disease Progression and Higher Viral Evolutionary Rate in HIV-2 Infection

Angelica A. Palm, Philippe Lemey, Marianne Jansson, Fredrik Månsson, Anders Kvist, Zsófia Szojka, Antonio Biague, Zacarias José da Silva, Sarah L. Rowland-Jones, Hans Norrgren, Joakim Esbjörnsson, Patrik Medstrand
Dimitrios Paraskevis, Editor
Angelica A. Palm
aDepartment of Laboratory Medicine, Lund University, Lund, Sweden
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Philippe Lemey
bDepartment of Microbiology and Immunology, Rega Institute, KU Leuven—University of Leuven, Leuven, Belgium
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Marianne Jansson
aDepartment of Laboratory Medicine, Lund University, Lund, Sweden
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Fredrik Månsson
cDepartment of Translational Medicine, Lund University, Lund, Sweden
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Anders Kvist
dDepartment of Clinical Sciences Lund, Lund University, Lund, Sweden
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Zsófia Szojka
eDepartment of Biochemistry and Molecular Biology, University of Debrecen, Debrecen, Hungary
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Antonio Biague
fNational Public Health Laboratory, Bissau, Guinea-Bissau
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Zacarias José da Silva
fNational Public Health Laboratory, Bissau, Guinea-Bissau
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Sarah L. Rowland-Jones
gNuffield Department of Medicine, NDM Research Building, University of Oxford, Oxford, United Kingdom
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Hans Norrgren
dDepartment of Clinical Sciences Lund, Lund University, Lund, Sweden
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Joakim Esbjörnsson
aDepartment of Laboratory Medicine, Lund University, Lund, Sweden
gNuffield Department of Medicine, NDM Research Building, University of Oxford, Oxford, United Kingdom
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Patrik Medstrand
cDepartment of Translational Medicine, Lund University, Lund, Sweden
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Dimitrios Paraskevis
Medical School, University of Athens
Roles: Editor
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DOI: 10.1128/mBio.01245-18
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  • FIG 1
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    FIG 1

    Kaplan-Meier curves of AIDS-free time. Three stratifications were explored (fast and slow progressors were defined by having values above or below the mean values from all participants for each stratification). (A) CD4% decline rate. (B) CD4% level at the midpoint in time between the first and last recorded CD4% values. (C) Combined effect of CD4% decline rate and CD4% level. Tick marks indicate participants with censored data. Asterisks indicate the time points in each group when five participants were still at mortality risk and at risk of developing AIDS. The numbers of individuals at risk are given below the figure panels at 5-year intervals. Data from faster progressors are shown in vermillion, and data from slower progressors are shown in blue.

  • FIG 2
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    FIG 2

    Synonymous and nonsynonymous divergence over time. Data represent accumulated synonymous and nonsynonymous divergences over time in the V1-C3 env region of HIV-2 for each study participant. The divergence from the level seen with the first analyzed sample from each study participant is shown. Data from faster progressors are shown in vermillion, and data from slower progressors are shown in blue.

  • FIG 3
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    FIG 3

    Codon-specific selective pressure. The selective pressures at each codon site of the sequence alignment of the env V1-C3 region of HIV-2 for faster and slower disease progressors are indicated. The proportions (y axis) with positive selection (vermillion or blue) or negative selection (gray) at codon sites of the sequence alignment (x axis) are shown for faster progressors (upper graph) and slower progressors (lower graph). Filled black circles indicate codons conserved between HIV-2/SIVsm strains associated with positive selection. Vertical lines divide the fragment into env regions V1V2, C2, V3, and C3.

Tables

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  • TABLE 1

    Disease progression classifications of all individuals, based on three different stratifications for CD4% (n = 16)

    IndividualCD4% decline rate/yearCD4% levelCombined coefficient
    ValueaProgressorbValueaProgressorbValuea,cProgressorb
    DL3405−1.46Slow33.95Slow1.00Slow
    DL35420.69Fast32.73Slow0.74Slow
    DL20511.61Fast31.11Slow0.62Slow
    DL28760.55Fast28.91Slow0.67Slow
    DL3654−0.15Slow27.74Slow0.70Slow
    DL2533−1.10Slow23.96Slow0.68Slow
    DL23161.10Fast23.45Fast0.50Fast
    DL2794−0.11Slow20.99Fast0.53Fast
    DL39413.40Fast20.65Fast0.29Fast
    DL23811.17Fast20.62Fast0.44Fast
    DL23350.58Fast20.41Fast0.47Fast
    DL36470.73Fast19.63Fast0.44Fast
    DL36460.33Slow19.32Fast0.46Fast
    DL3222−0.88Slow19.25Fast0.53Fast
    DL3740−0.69Slow17.57Fast0.48Fast
    DL23861.61Fast16.29Fast0.32Fast
    • ↵a Data represent individual values for the three different stratifications.

    • ↵b Individuals with values above or below the mean values determined for all individuals were grouped as faster or slower progressors, respectively.

    • ↵c The combined coefficient values represent a combination of CD4% decline rate and CD4% level. The combined coefficient values were obtained by transforming the CD4% decline rate values and CD4% level values, setting them to comparable scales, and subsequently multiplying them.

  • TABLE 2

    Evolutionary rates (10−3 codon substitutions/site/year) in the V1-C3 env regions determined using a strict clock hierarchical phylogenetic modela

    Genetic
    region
    All
    individualsc
    CD4% stratification
    CD4% decline rateCD4% level and the combined coefficientb
    Fast
    progressorsc
    Slow
    progressorsc
    Bayes factordFast
    progressorsc
    Slow
    progressorsc
    Bayes factord
    V1-C323.5 (20.3-26.6)24.7 (20.1-29.6)21.9 (19.1-24.9)0.328.6 (24.2-33.5)14.9 (12.2-17.6)20.3
    V1V229.5 (25.1-34.2)a30.1 (24.6-36.0)28.8 (23.7-34.0)0.335.4 (28.9-42.2)19.6 (14.8-24.7)11.8
    C218.0 (15.2-20.7)a18.6 (15.3-21.9)16.7 (13.9-19.5)0.321.5 (17.6-25.7)12.0 (9.2-15.2)28.4
    V321.2 (17.0-25.7)a21.6 (16.5-26.8)20.8 (15.7-25.9)0.324.1 (18.0-30.6)16.5 (11.0-22.2)2.4
    C326.6 (22.6-31.1)a27.0 (22.0-32.4)26.0 (21.6-30.6)0.230.4 (24.3-27.0)20.2 (15.2-25.8)6.1
    • ↵a P values for Wilcoxon signed rank tests for comparisons of rates between regions were as follows: for V1V2 versus C2, <0.001; for V1V2 versus V3, 0.002; for V1V2 versus C3, 1; for C2 versus V3, 0.005; for C2 versus C3, <0.001; for V3 versus C3, <0.001.

    • ↵b The combined coefficient values represent a combination of CD4% decline rate and CD4% level.

    • ↵c Data correspond to 10−3 codon substitutions per site per year (95% highest posterior density interval).

    • ↵d Bayes factor (BF) support for association between codon substitution rate and disease progression (faster versus slower progressors). BF >3 was considered evidence of a significant association.

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Low Postseroconversion CD4+ T-cell Level Is Associated with Faster Disease Progression and Higher Viral Evolutionary Rate in HIV-2 Infection
Angelica A. Palm, Philippe Lemey, Marianne Jansson, Fredrik Månsson, Anders Kvist, Zsófia Szojka, Antonio Biague, Zacarias José da Silva, Sarah L. Rowland-Jones, Hans Norrgren, Joakim Esbjörnsson, Patrik Medstrand for the SWEGUB CORE Group
mBio Jan 2019, 10 (1) e01245-18; DOI: 10.1128/mBio.01245-18

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Low Postseroconversion CD4+ T-cell Level Is Associated with Faster Disease Progression and Higher Viral Evolutionary Rate in HIV-2 Infection
Angelica A. Palm, Philippe Lemey, Marianne Jansson, Fredrik Månsson, Anders Kvist, Zsófia Szojka, Antonio Biague, Zacarias José da Silva, Sarah L. Rowland-Jones, Hans Norrgren, Joakim Esbjörnsson, Patrik Medstrand for the SWEGUB CORE Group
mBio Jan 2019, 10 (1) e01245-18; DOI: 10.1128/mBio.01245-18
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KEYWORDS

disease progression
human immunodeficiency virus
viral evolution

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