Classification of Metallothionein


P.-A. Binz, J.H.R. Kägi


A nomenclature system for metallothionein was first adopted in 1978 (Nordberg & Kojima 1979) and extended in 1985 by introducing a subdivision of all MTs into three classes (Fowler et al. 1987). By this convention Class I includes all proteinaceous MTs with locations of Cys closely related to those in the mammalian forms. Class II comprises proteinaceous MTs which lack this property. Class III subsumes metalloisopolypeptides containing gammaglutamyl-cysteinyl units resembling in their features proteinaceous MTs.

As the number of MT sequences has grown this subdivision has become inadequate. While keeping to the accepted definition of the MTs the length of their sequences, their amino acid compositions, the numbers and repartitions of the Cys are now known to be highly variable. In addition, the gene sequences now available often contain elements potentially related to functional properties of the MTs but not considered in the classification. Thus to differentiate the MTs better we are now proposing a new classification system based on sequence similarities and phylogenetic relationships. This system subdivides the MT superfamily into families, subfamilies, subgroups and isolated isoforms and alleles.

Definition of the metallothionein superfamily and its subdivisions.

As before, the metallothionein superfamily is defined phenomenologically as comprising all polypeptides which resemble equine renal metallothionein in several of their features (Nordberg & Kojima 1979, Fowler et al. 1987). Such general features are low molecular weight, high metal content, characteristic amino acid composition (high Cys content, low content of aromatic amino acid residues), unique amino acid sequence with characteristic distribution of Cys, i.e. Cys-X-Cys and spectroscopic manifest ations characteristic of metal thiolate clusters.

A MT family subsumes MTs which share a particular set of sequence specific characters. Members of a family can belong to only one family and are thought to be evolutionary related. The inclusion of an MT in a family presupposes that its amino acid sequence is alignable with that of all members. A common and exclusive sequence pattern, a profile and a phylogenetic tree can therefore be connected with each family. Each family is identified by its number and its taxonomic range. An example is Family 1 : vertebrate MTs.

A MT subfamily contains MTs which in addition to the family characters share a set of more stringent phylogenetic features. These extra criteria are usually specific monophyletic relationships among the sequences of proteins and/or of nucleotide se gments in the genes (5' or 3' untranscribed portion of the genes, 5' or 3' untranslated portions of the nucleotide sequences, exons, introns). If relevant other differentiating criteria can also be included, such as presence, conservation or repetition of sequence patterns. A subfamily is usually abbreviated with a letter character followed, if necessary, with an arabic number. An example is m1: mammalian MT-1.

A MT subgroup represents, as a result of statistically validated phylogenetic analyses, a branch of MT sequences of a subfamily which is clearly distinguishable in a tree by its monophyletic character. An example is m2U2: ungulate MT-2, subgroup of the m2 subfamily.

Isoforms or allelic forms are specifiable as members of subgroups, subfamilies and families. They are named using the nomenclature system defined in Kojima et al. (1997?), i.e. human MT-1E.

In addition, in cases where it is justifiable, one can define clans. A clan is a set of partial or total amino acid or polynucleotide sequences, subgroups, subfamilies, families or combinations of them which share characters not defined by the abov e classification criteria. They can be related to common spatial structure, thermodynamic properties, metal binding properties, functionally related characters or other relevant features. A clan is defined by the property common to its members. The abbrev iation should reflect this property.


Description of the MT subdivisions

The characteristics of all MT families and related subdivision are described in the following text. These characteristics are the criteria used for the classification of the MT sequences. A new sequence should match a majority of the criteria to be included into a family, a subfamily and eventually a subgroup.

Note. Code used for the description of the MREs in the 5'UT region: (1;3)+MRE(-100;-180) means between 1 and 3 MREs on the coding strand (+) between position 100 and 180 upstream of the origin of transcription.


Family 1 : vertebrate MTs

Its members are recognised by the sequence pattern K-x(1,2)-C-C-x-C-C-P-x(2)-C located at the beginning of the third exon
The taxonomic range of the members extends to vertebrates

Known characteristics: 60 to 68 AAs; 20 Cys (21 in one case), 19 totally conserved; the protein sequence is divided into two structural domains, containing 9 and 11 Cys all binding 3 and 4 bivalent metal ions, respectively. The gene is composed of 3 exons, 2 introns, the splicing sites are conserved;

Subfamilies: m1, m2, m3, m4, m, a, a1, a2, b, ba, t (update 12/19/97)

  • m1: mammalian MT-1
    AA alignment: 61-62 AA; 20 conserved Cys; usually over 80% identity; generally A at C-term; total charge between position 9 and 12: 0
    AA phylogenetic tree: forms ungulate, rodent and less clearly primate MT-1 subgroups, undistinguishable from m2
    introns: display similarity and similar length, very low similarity with other subfamilies
    5'UTR: monophyletic in tree containing m1 and m2
    5'UT: +MRE(-50);-MRE(-80);+(1;3)MRE(-100;-180)

  • m2: mammalian MT-2
    AA alignment: 61-61 AA; 20 conserved Cys; usually over 80% identity; A at C-term; total charge between position 9 and 12: -1
    AA phylogenetic tree: form ungulate, rodent and less clearly primate MT-2 subgroups, undistinguishable from m1
    introns: display similarity and similar length, very low similarity with other subfamilies
    5'UTR: monophyletic in tree containing m1 and m2
    5'UT: +MRE(-50);-(2;5)MRE(-60;-180);mixedMRE(-180;-300)

  • m3: mammalian MT-3
    AA alignment: 66-68 AA; 20 conserved Cys with other mammalian MTs, insert of 4-6 AA with basic residues near the C-term of the polypeptides; Q at C-term
    AA phylogenetic tree: form a monophyletic group
    introns: display similarity and similar length, very low similarity with other subfamilies
    5'UTR: different from other mammalian subfamilies
    5'UT: +MRE(-50);-MRE(-80)

  • m4: mammalian MT-4
    AA alignment: 62 AA; 20 conserved Cys with other mammalian MTs; P at C-term
    AA phylogenetic tree: form a monophyletic group
    introns: display similarity and similar length, very low similarity with other subfamilies
    5'UTR: different from other mammalian subfamilies
    5'UT: no MRE(-50;-MRE(-80)

  • m: n.d. mammalian MT
    mammalian MT uncompletely assignable to m1 or m2
    AA alignment: 60-61 AA; 20 conserved Cys with other mammalian MTs
    AA phylogenetic tree: belong to the cluster of mammalian subgroups
    introns: -
    5'UTR: -
    5'UT: at least 1 MRE between pos -40 and -200

  • a: n.d. avian MT
    AA alignment: 63 AA; 20 conserved Cys with mammalian MTs, Q insert after pos 3; P insert after pos 52; H at C-term
    AA phylogenetic tree: form separate groups
    introns: very low similarity to other vertebrate MTs
    5'UTR: -
    5'UT: -

  • a1: avian MT-1
    In addition to a:
    AA alignment: only one sequence; total charge between position 9 and 12: 0
    AA phylogenetic tree: -
    introns: -
    5'UTR: -
    5'UT: -

  • a2: avian MT-2
    In addition to a:
    AA alignment: very highly conserved sequence; total charge between position 9 and 12: -1
    AA phylogenetic tree: form a monophyletic group
    introns: -
    5'UTR: -
    5'UT: at least 1 +MRE(-50)

  • b: batracian MT
    AA alignment: 62 AA (one sequence); H at pos 49; N at C-term
    AA phylogenetic tree: show an isolated character with ba
    introns: -
    5'UTR: -
    5'UT: +MRE(-80);+MRE(-50)

  • ba: anura MT (new 12/19/97)
    AA alignment: 60 AA (one sequence); MDCAC at N-term; additional AA before pos 53 in vertebrate alignment; N at C-term
    AA phylogenetic tree: show an isolated character, with b
    introns: -
    5'UTR: -
    5'UT: -

  • t: teleost MT
    AA alignment: 60-61 AA; 19 Cys conserved with all other vertebrate MTs; Cys 55 instead of Cys 57; gap at pos 4
    AA phylogenetic tree: form a monophyletic group, can be considered as a rooting group for the vertebrate MTs
    introns: generally low and very low similarity between sequences of different suborders
    5'UTR: different from the mammals
    5'UT: +MRE(-50); generally -MRE(-80;-140)


    Family 2 : mollusc MTs

    Its members are recognised by the sequence pattern C-x-C-x(3)-C-T-G-x(3)-C-x-C-x(3)-C-x-C-K located at the Cterm of the sequence
    The taxonomic range of the members extends to molluscs

    Known characteristics: 64 to 75 AAs; 18 to 23 Cys, at least 13 totally conserved; the protein sequence is divided into two structural domains,

    Subfamilies: mo1, mo2, mog, mo

  • mo1: mussel MT-1
    AA alignment: 21 conserved Cys, over 90% similarity with other mo1, over 75% similarity with mo2
    AA phylogenetic tree: form a monophyletic group
    introns: -
    5'UTR: -
    5'UT: -

  • mo2: mussel MT-2
    AA alignment: 23 conserved Cys, 21 of them conserved with mo1, over 90% similarity with other mo2, over 75% similarity with mo1
    AA phylogenetic tree: form a monophyletic group
    introns: -
    5'UTR: -
    5'UT: -

  • mog: gastropod MTs
    AA alignment: 18 conserved Cys, all conserved with mo1 and mo2, contains a histone-like fragment of 6 to 8 AA at the N-term
    AA phylogenetic tree: form a monophyletic group
    introns: -
    5'UTR: -
    5'UT: -

  • mo: other mollusc MTs
    AA alignment: at least 18 Cys, high Cys conservation with the mo1, mo2, mog sequences,
    AA phylogenetic tree: - separate from mo1, mo2, mog
    introns: -
    5'UTR: -
    5'UT: -


    Family 3 : crustacean MTs

    Its members are recognised by the sequence pattern P-[GD]-P-C-C-x(3,4)-C-x-C located at the Nterm
    The taxonomic range of the members extends to crustaceans

    Known characteristics: 58 to 60 AAs; variants exist with and without the Nterm Met; 18 Cys totally conserved; the protein sequence is divided into two structural domains, containing each 9 Cys binding 3 bivalent metal ions;

    Subfamilies: c1, c2, c

  • c1: crustacean MT-1, c2: crustacean MT-2, c: other crustacean MT
    All sequences are very similar. c1 and c2 are forming two distinct monophyletic groups in the AA phylogenetic tree. Only protein sequences are known. c are crustacean MTs different from c1 and c2 based on phylogenetic analyses.


    Family 4 : echinodermata MTs

    Its members are recognised by the sequence pattern P-D-x-K-C-[V,F]-C-C-x(5)-C-x-C-x(4)-C-C-x(4)-C-C-x(4,6)-C-C located near the Nterm (updated 12/22/97)
    The taxonomic range of the members extends to sea urchins (echinodea)

    Known characteristics: 64 to 67 AAs; 20 Cys totally conserved; the protein sequence is divided into two structural domains, containing each 9 and 11 Cys binding 3 and 4 bivalent metal ions, respectively;

    Subfamilies: e1, e2

  • e1: echinoidea MT-1, e2: echinoidea MT-2
    e1 and e2: separate phylogenetic groups (AA sequences)


    Family 5 : diptera MTs

    Its members are recognised by the sequence pattern C-G-x(2)-C-x-C-x(2)-Q-x(5)-C-x-C-x(2)D-C-x-C
    The taxonomic range of the members extends to drosophila

    Known characteristics: 40 to 43 AAs; 10 conserved Cys

    Subfamilies: d1, d2

  • d1: diptera MT-1, d2: diptera MT-2
    d2 contain 2 Cys more than d1. Only one d2 is known until now


    Family 6: nematoda MTs

    Its members are recognised by the sequence pattern K-C-C-x(3)-C-C
    The taxonomic range of the members extends to secernentea

    Known characteristics: 62 and 74 AAs; 18 conserved Cys, contains one conserved tyrosine residue

    Subfamilies: n1, n2

  • n1: nematoda MT-1, n2: nematoda MT-2
    About 60% identity between n1 and n2; n2 is longer than n1


    Family 7: ciliata MTs

    No sequence pattern is defined since only one sequence is known
    The taxonomic range of the members extends to ciliata

    Known characteristics: 105 AAs, 31 Cys, multiple CCC pattern, one conserved tyrosine residue, fragment 1-57 and 58-105 shows 64% identity, with 14 conserved Cys

    Subfamilies: ci


    Family 8: fungi-I MTs

    Its members are recognised by the sequence pattern C-G-C-S-x(4)-C-x-C-x(3,4)-C-x-C-S-x-C
    The taxonomic range of the members extends to basidiomycotina, deuteromycotina, ascomycotina

    Known characteristics: 25 to AAs; 7 conserved Cys

    Subfamilies: f1


    Family 9: fungi-II MTs (Subfamily f2)
    Family 10: fungi-III MTs (Subfamily f3)

    The candida glabrata MT-1 and MT-2 are not clearly alignable. They display no reasonable similarity with each other and with any other protein sequences. They are assigned to separate families


    Family 11: fungi-IV MTs

    Its members are recognised by the sequence pattern C-X-K-C-x-C-x(2)-C-K-C
    The taxonomic range of the members extends to ascomycotina

    Known characteristics: 55 to 56 AAs; 9 conserved Cys; one CCC pattern; contain a number of unusual histidine and phenylalanine residues conserved in the N-terminal part of the sequence. This fragment does not contain any Cys

    Subfamilies: f4


    Family 12: fungi-V MTs (Subfamily f5)
    Family 13: fungi-VI MTs (Subfamily f6)

    Each of these families includes each only one sequence from yeast which cannot be aligned clearly with each other and with other protein sequences. They are assigned to separate families


    Family 14: prokaryota MTs

    Its members are recognised by the sequence pattern K-C-A-C-x(2)-C-L-C
    The taxonomic range of the members extends to cyanobacteria

    Known characteristics: 53 to 56 AAs; 9 conserved Cys; one conserved tyrosine residue; one conserved histidine residue; contain other unusual residues

    Subfamilies: pr


    Family 15: planta MTs

    Its members are recognised by the sequence pattern [YFH]-x(5,25)-C-[SKD]-C-[GA]-[SDPAT]-x(0,1)-C-x-[CYF] which yields all plant sequences, but also MTCU_HELPO and the non-MT ITB3_HUMAN
    The taxonomic range of the members extends to planta

    Known characteristics: 45 to 84 AAs; generally two Cys-rich regions (domain 1 and domain 3) separated by a Cys-poor region (domain 2); only the domain 2 contains unusual residues.

    Subfamilies: p1, p2, p2v, p3, pec, p21

  • p1: plant MT type 1
    AA alignment:
    consensus sequence of domain 1: C[sng]CGSsCxCG[sd]xC[ksn]Cxk
    consensus sequence of domain 3: GC[ks]CG[sda]xCxC[dn]PCNC
    AA phylogenetic tree: form a multiple group separate from p2
    introns: -
    5'UTR: -
    5'UT: -

  • p2: plant MT type 2
    AA alignment:
    consensus sequence of domain 1: SCCGGnCGCGsgCkCgnGCgGCkmy (updated 12/19/97)
    consensus sequence of domain 3: gCKCGsxC[kt]C[dn]PCxC
    AA phylogenetic tree: form a multiple group, separate from p1
    introns: -
    5'UTR: -
    5'UT: -

  • p2v: clan of variants to p2
    In addition to : p2
    AA alignment: additional or missing Cys in comparison to p2
    AA phylogenetic tree: belong to p2
    introns: -
    5'UTR: -
    5'UT: -

  • p3: plant MT type 3
    AA alignment:
    consensus sequence of domain 1: CGnCDCxDxxQCvKKG (updated 12/19/97)
    consensus sequence of domain 3: kCKCGxxCxCxxCxC
    AA phylogenetic tree: -
    introns: -
    5'UTR: -
    5'UT: -

  • pec: plant EC protein
    AA alignment:
    consensus sequence of domain 1: gCnDxCGCxxPCpGGxxCRC (uptade 12/19/97)
    consensus sequence of domain 2: HxtC[pgs]CGEHCgCnPCxC[pg] (uptate 12/19/97)
    consensus sequence of domain 3: [gn]C[tsr]CG[eat]xC[tna]CAsC (update 12/19/97)
    AA phylogenetic tree: forms one separate group
    introns: -
    5'UTR: -
    5'UT: -

  • p21: plant MT type 2x1
    AA alignment: the domain 2 is inexistant
    consensus sequence of domain 1: NCGCGSsCKCGDSCEKNY
    consensus sequence of domain 3: ECDnCSCGSNCscgxxcxc
    AA phylogenetic tree: forms one separate group
    introns: -
    5'UTR: -
    5'UT: -

    References:
    Kojima, Y., Binz, P.-A., Kägi, J.H.R. Nomenclature of Metallothionein: Proposal for a revision. (1999) In: Metallothionein IV, C. Klaassen (ed.), Birkhäuser Verlag Basel
    Binz, P.-A., Kägi, J.H.R. Metallothionein: Molecular evolution and classification. (1999) In: Metallothionein IV, C. Klaassen (ed.), Birkhäuser Verlag Basel, 7-13
    Nordberg M. & Kojima Y. (1979) Experientia. Suppl. 34, 48-55
    Fowler B.A., Hildebrand C.E., Kojima Y. & Webb M. (1987) Experientia Suppl. 52, 19-22


    Metallothionein homepage / MT links
    Pierre-Alain Binz
    Created 16th Sep. 97, last updated the 28th Oct. 1999