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Diversity and Function of Adaptive Immune Receptors in a Jawless Vertebrate

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Science  23 Dec 2005:
Vol. 310, Issue 5756, pp. 1970-1973
DOI: 10.1126/science.1119420
  • Fig. 1.

    Lamprey VLR diversity and gene rearrangement intermediates. (A) VLR scheme: signal peptide (SP), LRRNT, first LRR1, variable LRRV, end LRRVe, CP, and LRRCT (see text). Germline VLR-encoded portions of LRRNT and LRRCT are hatched. (B) Germline VLR gene rearrangement intermediates. Examples of LRR modules inserted from flanking cassettes into the germline gene: extensions of the VLR gene 5′ LRRNT (F.1 + R.1 amplicons); replacements and extensions of the VLR gene 5′ LRRCT (F.1 + R.2); and extensions of the VLR gene 3 ′ LRRCT (F.2 + R.3). Most insertions terminate with an incomplete LRR. Position of forward (F) and reverse (R) primers indicated; black, cDNA clones; red, genomic clones; red line in Int.36 indicates a 78-nucleotide noncoding DNA flanking the LRRVe. (C) 3D model of VLR diversity region. Positively selected solvent-exposed residues on the concave surface are represented by colored spheres: red, LRRNT; yellow, LRR1; blue, LRRV; white, LRRVe; green, β strands; magenta, α helices.

  • Fig. 2.

    Antigen recognition by lamprey VLR. Immune responses after weekly injections of anthrax spore coats at 4, 6, and 8 weeks. (A) Plasma VLR reactivity with B. anthracis spores compared with B. subtilis (control); plasma dilution 1:200. (B) Plasma VLR recognition of the spore coat protein BclA; two individuals per time point; control, plasma from 8-week stimulated larva reacted with unrelated protein.

  • Table 1.

    Distribution of unique and repeated adjoining pairs of LRR modules among 517 unique VLR sequences (the modules are shown in Fig. 1A).

    Number of pairs Adjoining pairs of LRR modules
    LRRNT LRR1 LRR1 LRRV LRRV LRRV LRRV LRRVe LRRVe CP CP LRRCT
    1 287 390 270 388 449 308
    2 22 5 3 16 29
    3 7 2 3 8
    4 4 1 4
    5 5 8
    6 1
    7 2 1
    8 2 2
    9 2 1
    10 2
    11 1 1
    13 1
    20 1
    21 1
    22 1 1
  • Table 2.

    Different LRR modules and those found only once in adjoining pairs among 517 unique VLR sequences. The distribution of LRRV modules per transcript is shown separately.

    Different LRR modules and uniquely paired combinations Distribution of LRRV modules per transcript
    Module Different (% total) Uniquely paired LRRV modules Cases
    LRRNT 235 (45) 196 0* 109
    LRR1 191 (37) 148 1 228
    LRRV 530 (78) 518 2 119
    LRRVe 353 (68) 335 3 45
    CP 71 (14) 54 4 6
    LRRCT 188 (36) 160 5 8
    6 1
    7 1
    Average 1.31
    • * VLR sequences with LRRVe modules but no LRRV.

  • Table 3.

    Average Ks and Ka among solvent-exposed and buried residues of the lamprey VLR (n = 517), hagfish VLR-A (n = 139), and hagfish VLR-B (n = 70). A ratio of Ka/Ks >1 indicates positive selection; Ka/Ks < 1 indicates purifying selection; and Ka/Ks ≅ 1 indicates neutral evolution. For Ks and Ka, standard error in parentheses.

    Site class Ks Ka Mode of selection
    Lamprey VLR
        Exposed residues on concave VLR surface 0.28 (0.03) 0.44 (0.05) Positive selection (Z = 2.61, p = 0.004)
        Exposed residues elsewhere on VLR surface 0.25 (0.02) 0.21 (0.03) Neutral evolution (Z = 1.55, p = 0.12)
        Buried residues 0.21 (0.02) 0.12 (0.02) Purifying selection (Z = 3.43, p = 0.001)
    Hagfish VLR-A
        Exposed residues on concave VLR surface 0.37 (0.05) 0.53 (0.05) Positive selection (Z = 3.63, p < 0.001)
        Exposed residues elsewhere on VLR surface 0.26 (0.03) 0.29 (0.03) Neutral evolution (Z = 0.37, p = 0.90)
        Buried residues 0.25 (0.03) 0.10 (0.02) Purifying selection (Z = 4.77, p < 0.001)
    Hagfish VLR-B
        Exposed residues on concave VLR surface 0.35 (0.04) 0.65 (0.02) Positive selection (Z = 8.37, p < 0.001)
        Exposed residues elsewhere on VLR surface 0.30 (0.03) 0.17 (0.03) Purifying selection (Z = 3.75, p < 0.001)
        Buried residues 0.32 (0.03) 0.09 (0.02) Purifying selection (Z = 8.72, p < 0.001)

Additional Files


  • Diversity and Function of Adaptive Immune Receptors in a Jawless Vertebrate
    Matthew N. Alder, Igor B. Rogozin, Lakshminarayan M. Iyer, Galina V. Glazko, Max D. Cooper, Zeev Pancer

    Supporting Online Material

    This supplement contains:
    Materials and Methods
    Figs. S1 and S2
    Tables S1 to S6
    References

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