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      c-type Lysozymes: what do their introns hide?

      Original article
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      ScienceOpen Research
      Life sciences, Lysozymes, Introns, Translation, Exons, Enzymes


            The introns of five c-type lysozymes were translated into amino acid sequences: parts of them corresponded to fragments of biologically active proteins. The amino acid sequences of translated introns seem to have a similar behavior as those arising from exons.

            Main article text


            Lysozyme (EC is a ubiquitous enzyme. Several different types have been characterized, chicken (c-), goose (g-), phage-, invertebrate (i-), plant-, bacterial-types (for reviews, see [1]). The most studied lysozymes were the c-type enzymes and nearly 100 amino acid sequences have been established [2]. These enzymes share a high degree of similarity in their primary and tertiary structures. Their mechanism of action is very similar: they are considered to be involved in the antibacterial defense mechanism and in certain groups of mammals (ruminants, colobine monkeys) c-type lysozyme was recruited in the stomach and became a digestive enzyme [3].

            Human lysozyme is synthesized in the secretory cells of a variety of exocrine glands and high concentrations were, as examples, detected in tears or mother's milk. The human lysozyme gene, its sequence organization and chromosomal localization have been described in detail by Peters et al. [4]. It is constituted by four exons and three introns. But other lysozyme genes have later been described as, for example, from hen (Gallus gallus) [5], rat (Rattus norvegicus) [6], cow (Bos taurus) [7], or pig (Sus scrofa) [8]. The present paper is devoted to their introns, more particularly to their amino acid sequences after translation which have so far not been studied.


            Translation and BLAST searches were performed according to Altschul et al. [9]. Hydrophobic cluster analysis (HCA) was achieved as described by Callebaut et al. [10].


            We were interested to investigate whether parts of lysozyme introns translated into amino acid sequences had closely related counterparts in biologically active, well-defined proteins: only longer sequences (30–45 amino acids) with E-values < 1 e-01, identities higher than 55% and satisfactorily HCA profiles were taken into consideration.

            Human lysozyme

            After translation, introns 1, 2, and 3 gave rise to peptide chains of 521, 646, and 284 amino acids, respectively. Only intron 1 (5′3′ frame 1 and frame 3) and intron 3 (3′5′ frame 2) had counterparts as defined above in various proteins. The presence of a Stop codon did not constitute an obstacle. Closely related fragments to translated intron 1 were present in human zinc finger protein (O14628), human serine/threonine-protein kinase Nek4 (P51957), human thromboxane A2 receptor (P21731), and human nitrogen-activated protein kinase 1 (O96J02). Table 1 illustrates these data when translated intron 1 is considered.

            Table 1.
            Comparison of translated human lysozyme intron 1, 5′3′ frame 1 (A and B) and frame 3 (C and D) fragments (first line) with part of biologically active proteins (third line).
            A) Human zinc finger protein (E = 2 e-08; Ident. = 74%)
            B) Human thromboxane A2 receptor (E = 3 e-05; Ident. = 65%)
              VSLCGP  WS  VA  S  LTATSA  Q  ILV  QP E  L  LQ
            C) Human serine/threonine-protein kinase NeK4 (E = 1 e-07; Ident. = 67%)
            SL     P   LECSG  I  AH  NL  LLGSSDS  ASA  VA   TGV    HH  Q
            D) Human mitogen-activated protein kinase kinase 1 (E = 7 e-05; Ident. = 69%)
            PRLECSG  IS  HCNL  L  GSS  S  ASA   VA   TG

            The numbers indicate the location of the fragment in the translated intron or in the protein.


            Corresponds to a Stop codon.

            Not only the sequences reported in Table 1 are related, but also the secondary structures as indicated in Figure 1 where HCA diagrams corresponding to closely related sequences (Table 1) are shown.

            Figure 1.
            Hydrophobic cluster analysis of (a) human lysozyme intron 1, 5′3′ frame 1 (only amino acids 50–300 are visualized); (b) zinc finger protein: residues 76–114 correspond to residues 210–248 of the intron (E = 6 e-08; identity: 76%); (c) human thromboxane A2 receptor: residues 328–368 correspond to residues 160–200 in the intron (E = 7 e-06; identity: 69%); (d) human neuronal thread protein: residues 252–319 correspond to residues 210–277 of the intron (E = 0.042; identity: 54%).

            It should be emphasized that a high number of other translated lysozyme intron sequences with lower E-values but nevertheless significant identities could be characterized in various proteins. All the peptides described above were situated in the first half of the translated introns 1 and 3 where was located an Alu sequence. We were thus interested to extend the study to c-lysozymes of other origins.

            Cow-, hen-, pig-, and rat lysozymes

            The genes of the four lysozymes contain again three introns; however, the latter were devoid of an Alu sequence. This did not prevent that after translation, but to a lesser extent, some sequences, generally shorter than in the case of human introns, corresponded to sequences contained in well-defined biologically active proteins: the identities were again around 60% but with more variable E-values. Some examples are quoted in Table 2.

            Table 2.
            Comparison of two translated rat intron and one translated pig intron lysozyme sequences with fragments of biologically active proteins. (For further details, see legend to Table 1.)
            Rat lysoyme, intron 2, 5′3′ frame 3 compared to ubiquitin-protein ligase Nedd-4 (E = 4 e-05; Ident. = 48%)
               G  PG  VTD  CE  PCGCWE   P     EEH   A     SS
            Rat lysozyme, intron 3, 3′5′ frame 1 compared to tumor necrosis factor ligand superfamily member 13B (B-cell activating factor) (E = 0.003; Ident. = 75%)
                 DV  LSAPPAPCLPGC   H
            Pig lysozyme, intron 1, 5′3′ frame 3 compared to major surface antigen precursor (E = 4.1; Ident. = 50%)
               FSW S  VP   QWF   L    P  W A


            The present data constitute a contribution to studies devoted to the amino acid sequences of translated introns. These sequences seem to have a similar behavior as those corresponding to exons when the occurrence of the different amino acids (hydrophilic and hydrophobic) as well as the secondary structures are considered. They demonstrate also that these intron sequences contain a high number of short but in some cases also long sequences corresponding to the parts of biologically active proteins.


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            2. , Animal lysozymes c and g: an overview, in Lysozymes, model enzymes in Biochemistry and Biology. Basel: Birkhäuser Verlag; 1996. pp. 9–31.

            3. , , Adaptive evolution in the stomach lysozymes of foregut fermenters. Nature. 1987;330(6146):401–4. [Cross Ref]

            4. , , , , The human lysozyme gene: sequence organization and chromosomal localization. Eur J Biochem. 1989;182(3):507–16. [Cross Ref]

            5. , , , Exons encode functional and structural units of chicken lysozyme. Proc Natl Acad Sci USA. 1980;77(10):5759–63. [Cross Ref]

            6. , , Evolution of rodent lysozymes: isolation and sequence of the rat lysozyme genes. Mol Phylogenet Evol. 1993;2(1):65–75. [Cross Ref]

            7. , , Characterization of the cow stomach lysozyme genes: repetitive DNA and concerted evolution. J Mol Evol. 1995;41(3):299–312. [Cross Ref]

            8. , Evolution of stomach lysozyme: the pig lysozyme gene. Mol Phylogenet Evol. 1996;5(2):298–308. [Cross Ref]

            9. , , , , , , Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):389–402. [Cross Ref]

            10. , , , , , , , Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cell Mol Life Sci. 1997;53(8):621–45. [Cross Ref]

            Competing Interests

            The author declare no competing interests.

            Publishing Notes

            © 2014 Pierre Jollès. This work has been published open access under Creative Commons Attribution License CC BY 4.0, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Conditions, terms of use and publishing policy can be found at www.scienceopen.com.

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            [1 ]Molécules de Communication, Museum National d'Histoire Naturelle, 63 rue Buffon, F 75005 Paris, France
            Author notes
            [* ]Corresponding author's e-mail address: pierre.jolles@ 123456wanadoo.fr
            © 2014 Pierre Jollès.

            This work has been published open access under Creative Commons Attribution License CC BY 4.0 , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Conditions, terms of use and publishing policy can be found at www.scienceopen.com .

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            Figures: 1, Tables: 2, References: 10, Pages: 3
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            Life sciences


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