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Microbial Immunity and Vaccines

Vaccine Potential of the Neisseria meningitidis 2086 Lipoprotein

Leah D. Fletcher, Liesel Bernfield, Vicki Barniak, John E. Farley, Alan Howell, Melissa Knauf, Peggy Ooi, Robert P. Smith, Paige Weise, Mike Wetherell, Xiaoling Xie, Robert Zagursky, Ying Zhang, Gary W. Zlotnick
Leah D. Fletcher
Wyeth Vaccines Research, Pearl River, New York 10965
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Liesel Bernfield
Wyeth Vaccines Research, Pearl River, New York 10965
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Vicki Barniak
Wyeth Vaccines Research, Pearl River, New York 10965
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John E. Farley
Wyeth Vaccines Research, Pearl River, New York 10965
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Alan Howell
Wyeth Vaccines Research, Pearl River, New York 10965
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Melissa Knauf
Wyeth Vaccines Research, Pearl River, New York 10965
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Peggy Ooi
Wyeth Vaccines Research, Pearl River, New York 10965
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Robert P. Smith
Wyeth Vaccines Research, Pearl River, New York 10965
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Paige Weise
Wyeth Vaccines Research, Pearl River, New York 10965
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Mike Wetherell
Wyeth Vaccines Research, Pearl River, New York 10965
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Xiaoling Xie
Wyeth Vaccines Research, Pearl River, New York 10965
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Robert Zagursky
Wyeth Vaccines Research, Pearl River, New York 10965
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Ying Zhang
Wyeth Vaccines Research, Pearl River, New York 10965
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Gary W. Zlotnick
Wyeth Vaccines Research, Pearl River, New York 10965
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  • For correspondence: zlotnig@wyeth.com
DOI: 10.1128/IAI.72.4.2088-2100.2004
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    FIG. 1.

    Phylogenetic tree showing the strain clustering according to 2086 protein distances. Subfamily A and B grouping is indicated on the main branches. The tree was constructed with LASERGENE software using ClustalW and was based on mature protein sequences of 254 to 262 amino acids in length. One representative strain and the respective group, type, and serosubtype from each cluster are shown. Boxes indicate 2086 strains chosen for expression studies. The group, type, and subtype of each neisserial isolate is indicated where available. Cluster identity for each of the 63 neisserial 2086 genes sequenced is listed in Table 1. Numbers in square brackets indicate the number of strains with ≥99.6% sequence identity present in each branch of the tree.

  • FIG. 2.
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    FIG. 2.

    Comparison of neisserial 2086 sequences. The amino acid sequences of 21 unique 2086 proteins were deduced from the nucleotide sequences and aligned with ClustalW. Dashes indicate gaps. Identical amino acid sequences are indicated by asterisks.

  • FIG. 3.
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    FIG. 3.

    Coomassie-stained gel after SDS-PAGE (10 to 20% gradient polyacrylamide). Lane 1, purified rLP2086-8529; lane 2, purified rLP2086-2996.

  • FIG. 4.
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    FIG. 4.

    Electron micrographs of N. meningitidis serogroup B strain H44/76 showing a whole cell. (A) Negative control; (B) immunogold labeling with rLP2086-8529-derived antiserum. Bar, 100 nm.

  • FIG. 5.
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    FIG. 5.

    FACS analysis of wild-type and knockout strains of N. meningitidis serogroup B labeled with homologous antiserum to rLP2086. (A) Labeling of three wild-type strains with homologous rLP2086 antiserum, with the negative control (week 0) shown as the light gray histogram and the positive antiserum (week 6) shown as a bold unfilled histogram. (B) Labeling of the knockout strains with the same antiserum and the same labels as for panel A, with a light gray histogram for the negative control and a bold line for the anti-rLP2086 serum. (C) Labeling of wild-type (dark gray, filled histogram) and knockout strains (bold unfilled histogram) with the homologous PorA monoclonal antibody specific for each serosubtype.

Tables

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  • TABLE 1.

    Description and origins of Neisserial strains used in this studya

    StrainSerogroup type:subtype2086 subfamilySourceLocation (country)2086 expression on Western blotPhylogenetic cluster
    M98 250670B:1:P1.4BMPHLUK+B8
    M98 250024B:1:P1.4BMPHLUK+B5
    M97 253524B:1:P1.4BMPHLUK+B8
    M97 252060B:1:P1.4BMPHLUK+B5
    M97 251870B:4z:P1.4BMPHLUK+B5
    M97 251854B:4z:P1.4AMPHLUK+A1
    M97 251836B:4z:P1.4BMPHLUK+B5
    M97 251830B:4z:P1.4BMPHLUK+B5
    M97 251905B:4z:P1.4BMPHLUK+B5
    M97 251898B:4z:P1.4BMPHLUK+B5
    M97 251885B:4z:P1.4BMPHLUK+B8
    M97 251876B:4z:P1.4BMPHLUK+B5
    M97 251994B:4z:P1.4BMPHLUK+B5
    M97 251985B:4z:P1.4BMPHLUK+B5
    M97 251957B:4z:P1.4BMPHLUK+B5
    M97 251926B:4z:P1.4BMPHLUK+B8
    M97 252045B:4z:P1.4BMPHLUK+ND
    M97 252038B:4z:P1.4BMPHLUK+ND
    M97 252026B:4z:P1.4BMPHLUK+ND
    M97 252010B:4z:P1.4BMPHLUK+ND
    M97 252098B:4z:P1.4BMPHLUK+ND
    M97 252083B:4z:P1.4BMPHLUK+ND
    M97 252078B:4z:P1.4BMPHLUK+ND
    M98 250735B:4z:P1.15BMPHLUK+ND
    M98 250797B:4z:P1.15BMPHLUK+ND
    M98 250768B:4z:P1.15BMPHLUK+ND
    M98 250622B:2b:P1.10AMPHLUK+A1
    M98 250572B:2b:P1.10AMPHLUK+A1
    M98 250716B:2b:P1.10AMPHLUK+A1
    M98 250699B:4z:P1.10BMPHLUK+ND
    M98 250393B:4z:P1.10BMPHLUK+ND
    M98 250173B:4z:P1.10BMPHLUK+ND
    M98 250771B:4z:P1.22,14AMPHLUK+A12
    M98 250732B:4z:P1.22,14-1AMPHLUK+A12
    CDC-1343B:NT:P1.22,14BCDCUS+B1
    CDC-2369B:NT:P1.22-1,14-1ACDCUS+A7
    6557B:7:P1.22-1,14ARIVMUS+A3
    M97 253462B:4z:P1.14BMPHLUK+ND
    CDC-1127B:NT:P1.7,16BCDCUS+ND
    CDC-982B4:P1.7,16BCDCUS+ND
    CDC-1359B4:P1.7,16BCDCUS+ND
    M98 250762B:15:P1.7,16BMPHLUK+ND
    M98 250610B:15:P1.7,16BMPHLUK+ND
    M98 250626B:15:P1.16BMPHLUK+ND
    M98 250809B:15:P1.7,16AMPHLUK+A2
    M97 253248B:15:P1.7,16AMPHLUK+A2
    M97 252029B:15:P1.7,16BMPHLUK+ND
    M97 251875B:15:P1.7,16-10BMPHLUK+ND
    CDC-798B:15:P1.7,16BCDCUS+ND
    CDC-1078B:15:P1.7,16BCDCUS+ND
    CDC-1614B:15:P1.7,16BCDCUS+ND
    CDC-1658B:15:P1.7,16BCDCUS+ND
    CDC-937B:15:P1.7,16BCDCUS+B4
    H44/76B:15:P1.7,16BRIVMNorway+B4
    M97 250571B:15:P1.16BMPHLUK+B4
    M97 252097B:15:P1.16BMPHLUK+B4
    M97 253092B:1:P1.6BMPHLUK+ND
    M97 252697B:1:P1.18,25,6AMPHLUK+A3
    M97 252988B:4:P1.18,25,6AMPHLUK+A3
    M97 252976B:4:P1.18,25,6AMPHLUK+A1
    M97 252153B:4:P1.18,25,6AMPHLUK+A11
    6940B:NT:P1.18,25,6BRIVMUS+B2
    CDC-1610B:4:P1.18-7,16-4ACDCUS+A3
    CDC-1521B:2b:P1.6ACDCUS+A1
    CDC-1985B:4:P1.7,13BCDCUS+ND
    CDC-1034B:4:P1.7ACDCUS+A5
    L6 M992B:NT:P1.7,1NDWalter Reed+ND/PICK>
    L8 M978B:15:P1.7,1AWalter Reed+A3
    CDC-1492B:4:P1.7,1ACDCUS+A3
    CDC-1573B:4:P1.7-1,1BCDCUS+B9
    L7 6155B:4:P1.7,1BWalter Reed+ND
    8529B:15:P1.7-2,3BRIVMChile+B4
    880049B:4:P1.7-2,4BRIVMNetherlands+B8
    870446B:4:P1.12-1,13ARIVMNetherlands+A2
    CDC-2367B:4:P1.15BCDCUS+B4
    H355B:15:P1.19,15BRIVMNorway+B4
    M982B:9:P1.22,9BRIVMUS+B6
    870227B:4:P1.5-3,10BRIVMNetherlands+B4
    B40A:NT:P1.5-3,10BRIVM+B5
    5315B:4:P1.5-3,10BRIVM+B5
    2996B:2b:P1.5-1,2-2ARIVMUS+A1
    NMBB:2b:P1.5-1,2-2AUIOWAUS+A1
    CDC-983B:2a:P1.5,2BCDCUS+B3
    L3 6275B:2a:P1.5,2AWalter Reed+A8
    CDC-852B:NT:P1.5,2BCDCUS+B7
    B16B6B:2a:P1.5,2ARIVM+A4
    L4 891C:NT:P1.21,16AWalter Reed+A6
    L5 M981B:4:P1.21-6,1AWalter Reed+A1
    CDC-1135B:NTACDCUS+A9
    A4A:NTB+B5
    C11C:16,P1.7-1,1ACDCGermany+A4
    YY:AWalter Reed+A4
    W135W135:AWalter Reed+A4
    Ng-FA1090AUNCUS+A10
    Nl-UR5AUR+ND
    Ns-UR4—UR−ND
    • ↵ a Strains are arbitrarily arranged by PorA serosubtype. The 2086 gene subfamily was determined by PCR screening as described in Materials and Methods. A dash indicates negative results; ND indicates not done. Country or origin of each neisserial isolate is listed where known. UK, United Kingdom; US, United States. The 2086 gene was sequenced from those strains where a phylogenetic cluster number based on amino acid sequence homology is indicated (see Fig. 1).

  • TABLE 2.

    Primers used in PCR amplification experiments

    Primer nameSequenceRestriction site (underlined)
    2086NDE5′-CTATTCTGCATATGACTAGGAGC-3′NdeI
    3STP20865′-GCGCGGATCCTTACTGCTTGGCGGCAAGACC-3′BamHI
    5UNI20865′-CTATTCTGCGTATGACTAG-3′NAa
    3UNI20865′-GTCCGAACGGTAAATTATCGTG-3′NA
    5INT20865′-TGCCGATGCACTAACCGCACC-3′NA
    3INT20865′-CGTTTCGCAACCATCTTCCCG-3′NA
    5OUT20865′-GACAGCCTGATAAACC-3′NA
    3OUT20865′-GATGCCGATTTCGTGAAC-3′NA
    N2086ILE5′-GCGCAGATCTCATATGAGCAGCGGAGGGGGTGGTGTCGCCGCCGAYATWGGTGCGGGGCTTGCCG-3′BglII/NdeI
    20863STP5′-GAGATCTCACTCACTCATTACTGCTTGGCGGCAAGACCGATATG-3′BglII
    N1573PCR5′-GAGATCTCATATGAGCAGCGGAGGCGGCGGAAGC-3′BglII
    N29963STP5′-GAGATCTCACTCACTCACTACTGTTTGCCGGCGATGCCGATTTC-3′BglII
    5LIP20865′-GCGGATCCAGCGGAGGGGGTGGTGTCGCC-3′BamHI
    3SPH20865′-GCGCATGCTTACTGCTTGGCGGCAAGACCGATATG-3′SphI
    5LIP15735′-GCGGATCCAGCGGAGGCGGCGGAAGC-3′BamHI
    5LIP29965′-GCGGATCCAGCGGAGGCGGCGGTGTCGCC-3′BamHI
    N2996SPH5′-GCGCATGCCTACTGTTTGCCGGCGATG-3′SphI
    5LIP7715′-GCGGATCCAGCGGAAGCGGAAGCGGAGGCGGCGGTGTCGCC-3′BamHI
    PorABg12Fwd5′-CGCGAGATCTCATATGGATGTCAGCCTATACGGCGAAATCAAAGCCGGCGTGGAAGGCAGGAACTACCAG-3′BglII/NdeI
    PorABg12Ter5′-CGCGAGATCTTCAGTCACTCATTAGAATTTGTGGCGCAAACCGACG-3′BglII
    • ↵ a NA, not applicable.

  • TABLE 3.

    Whole-cell ELISA and bactericidal titers of mouse antibodies raised against rLP2086 tested against multiple serogroup B meningococcal strains

    Test strainTest strain serosubtyperLP2086-8529 anti- sera (subfamily B)rLP2086-2996 anti- sera (subfamily A)
    Whole-cell ELISA titeraBC50 titerbWhole-cell ELISA titeraBC50 titerb
    Subfamily B
        539P1.7-2,3>1,458,0003,200——
        H44/76P1.7,16>1,458,0003,20056,386<25
        H355P1.19,15>1,458,0003,200——
        CDC-937P1.7-2,3-4>1,458,000>800——
        M97 252097P1.7-2,16>1,458,000>800——
        6940P1.18,25,6900,162>80011,157—
        M982P1.22,9435,9092006,424—
        880049P1.7-2,4349,91240010,588—
        CDC-1573P1.7-1,1102,508257,871—
    Subfamily A
        870446P1.12-1,13389,829800>1,458,000>800
        M98 250771P1.22,14139,397<25447,867800
        M98 250732P1.22,14-123,928—241,510>800
        M97 252697P1.18,25,699,580—320,732>800
        6557P1.22-1,1425,590<2577,319<25
        NMBP1.5-1,2-2<2,000<258,979<25
    • ↵ a Endpoint titers expressed as the reciprocal of the dilution at absorbance = 0.1.

    • ↵ b Bactericidal (BC50) titers are represented as the reciprocal of the dilution of antiserum that reduced viable cell count by 50%. Week 0 normal mouse sera had BC50 titers of <25. A dash indicates samples were not tested.

  • TABLE 4.

    rLP2086 elicits greater bactericidal antibody than rP2086 in mice

    AntigenTest strain titera
    H44/76M97 252697
    rP2086-8529 (nonlipidated)200—
    rLP2086-8529 (lipidated)3,200—
    rP2086-1573 (nonlipidated)<25—
    rLP2086-1573 (lipidated)200—
    rP2086-2996 (nonlipidated)—<25
    rLP2086-2996 (lipidated)—>800
    • ↵ a Bactericidal (BC50) titers represented as the reciprocal of the dilution of antiserum that reduced the viable cell count by 50%. Week 0 normal mouse serum had BC50 titers of <50. A dash indicates samples were not tested.

  • TABLE 5.

    Purified rLP2086 from subfamily A or subfamily B elicits bactericidal antibodies in mice which are bactericidal against several strains of serogroup B N. meningitidis

    AntigenTitera
    Subfamily B test strainsSubfamily A test strains
    H44/7688004915736940M982870446M98 250771M98 250732M97 252697
    Subfamily B
        rLP2086-85293,200400<25>800200800<25——
        rLP2086-880049400>800100400200400———
        rLP2086-1573200>80080020010050———
        rLP2086-M982>800>800<25200>800400———
    Subfamily A
        rLP2086-2996<25————>800800>800>800
        rLP2086-870446—————>800400400400
        rLP2086-250771—————>800>800>800>800
        rLP2086-252988—————>800>800>800>800
        rLP2086-C11—————>800200200400
    • ↵ a Bactericidal (BC50) titers represented as the reciprocal of the dilution of antiserum that reduced viable cell count by 50%. Week 0 normal mouse sera had BC50 titers of <50. A dash indicates samples were not tested.

  • TABLE 6.

    Antisera from mice immunized with mixtures of rLP2086 variants and rPorA are bactericidal against multiple strains of serogroup B meningococcal strains

    Test strainBactericidal titer
    rLP2086 monovalent controlarPorA monovalent controlbrLP2086-8529 + rLP2086-2996rLP2086-8529 + rLP2086-2996 + rP1.22-1,14 + rP1.5-1,2-2
    H44/76>800—>800>800
    6940>800—>800800
    880049200—200100
    M982400—400200
    870446>800—>800>800
    M98 250771800—800400
    M98 250732>800—>800400
    M97 252697>800—>800>800
    6557<25800<25200
    NMB<25>800—>800
    • ↵ a The monovalent control for subfamily B strains H44/76, 6940, 880049, and M982 was mouse antiserum raised against rLP2086-8529, and the monovalent control for subfamily A strains 870446, M98 250771, M98 250732, M97 252697, 6557, and NMB was mouse antiserum raised against rLP2086-2996.

    • ↵ b The rPorA monovalent control for strain 6557 was mouse antiserum raised against rP1.22-1,14-1, and the monovalent control for NMB was mouse antiserum raised against rP1.5-1,2-2. A dash indicates samples were not tested.

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Vaccine Potential of the Neisseria meningitidis 2086 Lipoprotein
Leah D. Fletcher, Liesel Bernfield, Vicki Barniak, John E. Farley, Alan Howell, Melissa Knauf, Peggy Ooi, Robert P. Smith, Paige Weise, Mike Wetherell, Xiaoling Xie, Robert Zagursky, Ying Zhang, Gary W. Zlotnick
Infection and Immunity Mar 2004, 72 (4) 2088-2100; DOI: 10.1128/IAI.72.4.2088-2100.2004

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Vaccine Potential of the Neisseria meningitidis 2086 Lipoprotein
Leah D. Fletcher, Liesel Bernfield, Vicki Barniak, John E. Farley, Alan Howell, Melissa Knauf, Peggy Ooi, Robert P. Smith, Paige Weise, Mike Wetherell, Xiaoling Xie, Robert Zagursky, Ying Zhang, Gary W. Zlotnick
Infection and Immunity Mar 2004, 72 (4) 2088-2100; DOI: 10.1128/IAI.72.4.2088-2100.2004
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KEYWORDS

Antigens, Bacterial
Bacterial Proteins
lipoproteins
Meningococcal Vaccines
Neisseria meningitidis, Serogroup B

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