`Superfast' or masticatory myosin and the evolution of jaw-closing muscles of vertebrates
Department of Physiology and Institute for Biomedical Research, F13, University of Sydney, NSW 2006, Australia
e-mail: joeh{at}physiol.usyd.edu.au
Accepted 13 May 2002
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Summary |
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Key words: jaw muscle, fibre type, muscle contraction, mastication, myosin isoform, masticatory myosin, evolution, molecular phylogeny
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Molecular physiology of myosin |
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Myosin controls the kinetics of energy transduction from ATP and, through
it, the kinetic properties of muscles. The speed of contraction of a muscle is
proportional to the ATPase activity of its myosin
(Bárány, 1967).
As the maximal stresses of fast and slow muscles are approximately the same,
muscle power (force x velocity) is also dependent on myosin ATPase
activity. High muscle speed and power may confer an evolutionary advantage to
an organism, as in escaping from predators or chasing prey. However, skeletal
muscles constitute some 45 % of the body mass of vertebrates and are the
greatest consumers of energy in the body, the bulk of which is spent in
cross-bridge cycling. The benefit of high muscle speed is balanced by the high
energy cost and the need for high caloric intake. Muscles are sometimes used
at low speed or to produce sustained tension. The energy cost for tension
maintenance is then inversely related to speed and myosin ATPase activity. It
is therefore advantageous for an organism to be able to use fast muscles when
the occasion demands it and to use slower ones in less demanding situations.
It is thus not surprising that 10 different striated muscle MyHC isoforms with
different functional characteristics exist in the mammalian genome.
The expression of these MyHCs in adult limb, jaw-closer and extraocular
muscles is shown in Table 1.
Two major subclasses of vertebrate MyHCs are currently recognized: (i) the
fast subclass, which includes IIA, IIX, IIB, embryonic, foetal and
extraocular, and (ii) the cardiac subclass, which includes slow/ß-cardiac
and -cardiac. The genes encoding these subclasses of MyHC are clustered
in chromosomes 17 and 14, respectively, in the human genome
(Schiaffino and Reggiani,
1996
; Weiss et al.,
1999
). Masticatory MyHC (see below) and probably also the
slow-tonic MyHC, which is yet to be cloned, are also distinct subclasses. The
10 MyHC isoforms cater for the wide range of functional demands on muscles in
different parts of the body. These isoforms greatly help to optimize
contractile functions of different organs while minimizing energy use.
|
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Fibre types and their myosins in locomotory muscles |
---|
Individual locomotory muscles in both eutherian
(Lucas et al., 2000) and
marsupial (Zhong et al., 2001
)
mammals are composed of some or all of these four basic fibre types in
different proportions. These fibre types show physiological plasticity
(Pette and Staron, 1997
),
fibres of one type can be converted to those of another type by neural and
hormonal influences. Properties of locomotory fibres also vary among species;
small animals compensate for their size by having faster muscles
(Close, 1972
;
Rome et al., 1990
). This is
achieved largely by increasing the ATPase activity of each myosin isoform as
body size decreases, but changes in fibre type profile also play a part. This
is exemplified by the soleus muscle, which is composed almost entirely of slow
fibres only in cats and rabbits, but acquires a large proportion of IIa fibres
in small animals such as rodents. In very small mammals, e.g. shrews, slow
fibres are completely replaced by fast ones
(Savolainen and Vornanen,
1995
). At the other end of the body size spectrum, the fastest IIb
fibres are absent from carnivores (Snow et
al., 1982
; Lucas et al.,
2000
) and primates (Smerdu et
al., 1994
; Lucas et al.,
2000
). Thus, the four MyHCs found in locomotory muscles of mammals
appear to be more than adequate for coping with the locomotory demands in
diverse species. Fibre types in locomotory muscles show only a minimal degree
of phylogenetic plasticity.
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Jaw-closing muscles have a high degree of phylogenetic plasticity |
---|
Rodents and ruminants are examples of the first group. The jaw closers of
the rat have the four fibre types found in limb muscles
(Sfondrini et al., 1996);
those of the hedgehog are probably similar, since their fibres are
histochemically similar to limb fibres
(Lindman et al., 1986
).
Jaw-closer fibres of sheep and cattle are homogeneously slow
(Mascarello et al., 1979
;
Kang et al., 1994
). Among the
second group of animals are rabbits, whose jaw closers contain
-cardiac
fibres in addition to slow and IIa fibres
(Bredman et al., 1991
;
English et al., 1999
). Human
jaw closers have fibres co-expressing
-cardiac and foetal MyHCs in
addition to slow, IIa and IIx fibres
(Korfage and Van Eijden,
2000
), while fibres of jaw closers of kangaroos are homogeneously
-cardiac (Hoh et al.,
2000
). Of considerable importance is the fact that jaw closers of
carnivores and several other orders of mammal (see below) have fibres which
express a highly jaw-specific `superfast' or masticatory MyHC
(Rowlerson et al., 1983b
). As
a final example of the extraordinary degree of phylogenetic plasticity,
marsupial possums have jaw-closer fibres that express masticatory MyHC as well
as
-cardiac fibres (J. F. Y. Hoh and L. H. D. Kang, unpublished
observations).
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Properties of masticatory myosin and fibre type |
---|
Masticatory MyLC-2 (Qin et al.,
1994) and MyHC (Qin et al.,
2002
) from cat jaw muscle have been cloned in this laboratory.
Both genes show low homology (less than 70 % sequence identity) with known
homologues in mammalian striated muscles. Analysis of nucleotide substitution
rates between non-synonymous sites revealed that rates between cat masticatory
MyHC and members of mammalian fast and cardiac subclasses are almost twice
those between mammalian fast and cardiac isoforms themselves
(Qin et al., 2002
).
A phylogenetic tree comprising invertebrate and vertebrate MyHC sequences
revealed that the masticatory MyHC gene was the first among vertebrate MyHC
genes to diverge from other vertebrate MyHC genes. Next to diverge was the
chicken ventricular MyHC. Subsequently, the two major subclasses of MyHC,
cardiac and fast skeletal, diverged from each other
(Qin et al., 2002). It is of
interest that the mammalian slow/ß-cardiac and
-cardiac genes
group with the quail slow skeletal MyHC gene rather than with the chicken
ventricular MyHC. Fluorescence in situ hybridization analysis
revealed that the masticatory MyHC gene is present in the human genome and is
located at 7q22, a site different from the locations of the fast skeletal and
cardiac MyHC genes. These results show that masticatory MyHC is of very
ancient origin and that this gene should be considered as a distinct subclass
of vertebrate MyHC genes (Qin et al.,
2002
). In the light of these findings, it is inappropriate to call
this myosin (and fibre type) IIM (Rowlerson et al.,
1983a
,b
),
with the connotation that it belongs to the fast subclass. The finding that
the shark expresses masticatory MyHC (see below) suggests that this gene
diverged more than 400x106 years ago.
Masticatory fibres in the cat express other jaw-specific isoforms of
myofibrillar proteins besides the unique MyHC and MyLCs. An isoform of
-tropomyosin different from those in limb muscles has been resolved in
two-dimensional gels (Rowlerson et al.,
1983a
). This isoform differs in cyanogen bromide peptide map from
the
-tropomyosins in fast and slow limb muscle fibres
(Hoh et al., 1989
). Unlike its
equivalent in limb muscle fibres, the jaw-specific
-tropomyosin is not
coexpressed with ß-tropomyosin. There is also a jaw-specific isoform of
myosin binding protein C (Hoh et al.,
1993
), which is immunochemically distinct from the fast and slow
isoforms in limb muscles (Dhoot et al.,
1985
). Fibres of jaw closers in the cat
(Hoh et al., 1991
) and rat
(Sfondrini et al., 1996
) have
been shown to have physiological plasticity.
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Distribution of masticatory myosin expression in jaw muscles of vertebrates |
---|
This laboratory has broadened the distribution of masticatory myosin
expression by the use of a battery of 32 monoclonal antibodies against cat
masticatory MyHC. Animals whose jaw closers were shown to react with the
majority of these antibodies include six out of seven species of chiropteran
(bats and flying foxes) examined (Kang et
al., 1994), the Indopacific crocodile
(Hoh et al., 2001
), three
species of dasyurid (marsupial carnivores), two species of diprotodont
(ringtail and brushtail possums) and one species of shark (J. F. Y. Hoh and L.
H. D. Kang, unpublished observations). Of the 32 monoclonal antibodies, 15-17
reacted specifically with marsupial jaw closers and 12-13 with jaw closers of
the crocodile and the shark. Five monoclonal antibodies, including 2F4
described previously (Kang et al.,
1994
), reacted specifically with jaw closers of all species
studied. The known distribution of masticatory MyHC expression among
vertebrate species is summarized in Table
2.
|
It is of considerable interest that, among several orders of mammals shown
to express masticatory myosin, there are species that deviate from this
phenotype. Thus, among carnivores, masticatory myosin was not expressed in the
lesser panda (Rowlerson et al.,
1983b), which is no longer carnivorous. Among primates, humans do
not express masticatory myosin (Rowlerson
et al., 1983b
) although they have the gene, possibly associated
with the fact that the human diet has softened since the consumption of cooked
food during recent human evolution. Among microbats, Miniopterus
schreibersii is exceptional in expressing limb fast myosin rather than
masticatory myosin (Kang et al.,
1994
). Among marsupial mammals, jaw closers in possums contain a
mixture of masticatory and
-cardiac fibres, but those in macropods,
which belong to the same order (Diprotodontia), have 100 %
-cardiac
fibres with no trace of masticatory MyHC or MyLC expression
(Hoh et al., 2000
). These
known deviations from masticatory MyHC expression can be viewed as examples of
recent evolutionary adaptations of jaw muscles in response to changes in diet
or feeding pattern, and attest to the phylogenetic plasticity of jaw-closing
muscles.
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Mechanical properties of fibres expressing masticatory myosin |
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The kinetics of cross-bridge cycling during isometric contraction can be
studied by imposing small-amplitude length perturbations over a range of
frequencies (Rossmanith,
1986), such analysis yielding a parameter,
fmin, the frequency at which the dynamic stiffness of the
active fibre is a minimum. The value of this parameter is related to the
kinetics of cycling of cross-bridges
(Rossmanith and Tjokorda,
1998
) and is a useful index of fibre kinetics. For example,
analysis of the three types of fibre from rabbit fast limb muscle gave
fmin values in the range 10-26 Hz, while extraocular
muscle fibres gave values ranging from 4 to 33 Hz. This result reflects the
wider diversity of MyHCs expressed in this muscle, which includes embryonic,
foetal and extraocular MyHCs not found in limb fibres
(Li et al., 2000
). Using this
method of analysis, fmin of skinned cat masticatory and
limb fast (IIa, IIx) fibres were both in the range 10-13 Hz, and the mean
values for the two types of fibre were not significantly different (Z. B. Li,
J. F. Y. Hoh and G. H. Rossmanith, unpublished observations). In terms of a
three-state model of cross-bridge function, this observation implies that the
power stroke and detachment rates of cross-bridges in masticatory and limb
fast fibres do not differ (Rossmanith and
Tjokorda, 1998
). These results do not support the notion that
masticatory fibres are faster than limb fast fibres.
Recently, the maximal velocity of shortening (Vmax) of
dog masticatory fibres has been compared with values for fast and slow limb
fibres in the same animal (P. Reiser, personal communication). The
Vmax of masticatory fibres was found to lie midway between
the values for limb fast and slow fibres. Thus, mechanical analyses of single
masticatory fibres by various methods have surprisingly provided no evidence
that masticatory fibres are faster than limb fast fibres, as expected on the
basis of the Bárány
(1967) relationship between
myosin ATPase and muscle speed. It is no longer justified to refer to
masticatory myosin and fibre type as `superfast'. A truly superfast muscle has
been described: the swim bladder muscle of the toad fish
(Rome et al., 1999
). This
muscle develops a high speed of contraction at the cost of low force
production and does not cross-react with anti-masticatory MyHC antibodies. In
contrast, masticatory muscle is a moderately fast muscle capable of developing
high force at the expense of high ATPase activity and tension cost. The
moderate speed and high force characteristics make jaw closers powerful in
animals that express masticatory myosin. These characteristics are very
appropriate in carnivores, to cater for their predatory lifestyle, and in
frugivores (flying foxes) and certain folivores (possums, opposums and
primates), for the mastication of tough vegetable matter.
The failure of masticatory myosin to comply with the Bárány
relationship requires some comment. Bárány's
(1967) correlation between
myosin ATPase activities and muscle speeds was derived from data on limb fast
and slow myosins of animals of various sizes. It is likely that the slope of
the Bárány relationship is MyHC-isoform-specific. The unique
functional characteristics of masticatory fibres may be associated with
unusual combinations of rate constants in different parts of the cross-bridge
cycle. A very rapid cross-bridge attachment rate coupled with a moderate
detachment rate may help to explain the high maximal stress in these
fibres.
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Structure and function of mammalian cardiac myosins |
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Expression of cardiac myosins in mammalian jaw muscles |
---|
The -cardiac MyHC is expressed in fibres of jaw closers in the
rabbit (Bredman et al., 1991
;
English et al., 1999
), in four
species of kangaroo (Hoh et al.,
2000
) and weakly in humans
(Bredman et al., 1991
). In the
rabbit,
-cardiac fibres constitute approximately one-third of the fibre
population, the rest being slow/ß-cardiac and IIa fibres. Mechanical
analysis of single
-cardiac fibres of this muscle revealed that the
maximal speed of shortening of these fibres lies between those of fast IIa
fibres and the slow/ß-cardiac fibres in the same muscle
(Sciote and Kentish, 1996
). In
kangaroos, 100 % of jaw closer fibres are
-cardiac, and this stands in
sharp contrast to the homogeneously slow fibres in eutherian grazers, which
feed essentially on the same diet. In common with sheep and cattle, kangaroos
are also foregut fermenters, but they are not ruminants and, unlike them, have
a large, simple stomach (Dawson,
1995
). A difference in kinetic property of jaw fibres between
eutherian and marsupial grazers is expected because
-cardiac MyHC is
associated with a higher rate of cross-bridge cycling compared with
ß-cardiac MyHC. The appropriateness of
-cardiac fibres in
kangaroos may lie in the fact that, with their presumed higher speed and
power,
-cardiac fibres ensure rapid comminution of food into fine
particles necessary for efficient fermentation prior to passage through the
buccal cavity.
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Evolution of mammalian ![]() |
---|
It is well established that the gene for ß-cardiac MyHC in eutherians
is expressed in slow skeletal muscle fibres
(Lompre et al., 1984), and
this gene is thus more appropriately referred to as the gene for
slow/ß-cardiac MyHC. The recent finding that ß-cardiac MyHC is also
expressed in marsupial slow skeletal muscle fibres
(Hoh et al., 2000
) suggests
that the expression of this MyHC gene in skeletal muscle must predate the
divergence of these two subclasses of mammal. This raises the intriguing
question as to whether the gene for ß-cardiac MyHC was originally a
skeletal muscle gene which evolved a mechanism for expression in cardiac
muscle, or vice versa.
Features of the phylogenetic tree of vertebrate MyHCs referred to above
(Qin et al., 2002) are helpful
here. The tree suggests that mammalian
- and ß-cardiac MyHC genes
and the quail slow skeletal MyHC gene shared a common ancestral gene. Further,
the mammalian slow/ß-cardiac MyHC gene is more closely related to quail
slow skeletal MyHC than to chicken ventricular MyHC. A likely scenario for the
evolution of these MyHCs is that mammalian slow/ß-cardiac MyHC evolved
from an ancestral slow limb MyHC and, further, that it duplicated in the
course of mammalian evolution to give rise to the
-cardiac MyHC gene.
These genes subsequently evolved cardiac-chamber-specific expression
(
-cardiac in the atrium,
-cardiac and slow/ß-cardiac in the
ventricle), and thyroid-sensitivity in the ventricle. The
-cardiac MyHC
acquired faster kinetics, presumably driven by the evolutionary advantages of
being better able to cope with the thermogenic effect of thyroid hormones.
Having thyroid-sensitive cardiac myosin genes permits individual mammals in
their lifetime to modify their cardiac function to cope with the metabolic
demands of a low ambient temperature. This ability enables mammals to extend
their habitats to higher latitudes and altitudes than would otherwise be
possible. In contrast to the evolution of masticatory MyHC (see below), the
infrequent expression of -cardiac MyHC in jaw muscles of mammals is
unlikely to have played a significant role in driving the evolution of this
gene.
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Evolution of mastication and jaw-closing muscles |
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With the evolution of gnathostomes from agnathous fish approximately 400x106 years ago, duplicates of pre-existing MyHC, MyLC-1, MyLC-2 and other myofibrillar genes became jaw-specific in expression and subsequently diverged as the masticatory MyHC, MyLCs and other jaw-specific genes, driven by the survival advantage of powerful jaw closure. The carnivorous lower vertebrates, including the reptilian ancestors of mammals, advantageously expressed masticatory myosin genes in jaw muscles. Early mammals, both marsupial and eutherian, continued to express masticatory myosin, this feature representing a primitive or undifferentiated phenotype. During the mammalian radiation into their various ecological niches that followed the demise of the dinosaurs approximately 65x106 years ago, mastication of food became progressively more important, and rapid evolutionary changes in the masticatory apparatus, including changes in muscle fibre types, took place. Early during mammalian radiation, some taxa (carnivores, chiropterans, primates, most marsupial orders) retained masticatory myosin expression where high force and power in jaw closers remained functionally advantageous to their life style. Others (rodents, ungulates, rabbits) replaced masticatory myosin with functionally more appropriate isoforms normally expressed in limb muscles or the heart. With further diversification and adaptation to diet and feeding habits in more recent times, the ancestors of certain members of mammalian orders previously expressing masticatory myosin (lesser panda, Miniopterus schreibersii, kangaroos and humans) also deviated by expressing limb, developmental or cardiac myosins in their jaw closers.
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What makes jaw-closing muscles so unique? |
---|
Skeletal muscle myogenesis is controlled by the sequential expression of
the MyoD family of genes
(Rudnicki and Jaenisch, 1995).
The same genes are used to control myogenesis of craniofacial muscles and
somitic muscles. These genes induce in jaw closers the expression of embryonic
and foetal myosins during development (Hoh
et al., 1988
; Shelton et al.,
1988
; Hoh and Hughes,
1989
) and regeneration (Hoh
and Hughes, 1988
), in common with limb muscles, but the mature
fibre phenotypes are distinct and species-specific. There presumably are
allotype-specific muscle determination genes regulating the expression of
MyoD family members. This suggestion is strongly supported by the
work of Tajbakhsh and coworkers, who showed that, in
Pax-3/Myf-5 doublemutant mice, limb and trunk muscles were
absent while craniofacial muscles developed normally
(Tajbakhsh et al., 1997
). This
clearly shows that Pax-3 is specific for myogenesis within the
limb/trunk allotype, not in craniofacial allotypes where, presumably, some
other genes regulate the MyoD family of genes. A Hox gene called
engrailed is specifically expressed in jaw muscle precursor cells
(Hatta et al., 1990
), but it is
not known whether engrailed is in the pathway for the determination
of the jaw muscle allotype.
Jaw closers present interesting questions in muscle phenotype control. What
trans-acting factors are involved in the regulation of masticatory
MyHC, MyLCs and other masticatory fibre-specific myofibrillar genes? Are these
factors also involved in the regulation of -cardiac MyHC and limb
myofibrillar proteins in jaw closers? Are limb-like fibres in jaw closers
regulated by the same regulatory pathways as limb fibres? Identification of
cis-acting elements of myofibrillar genes and trans-acting
factors involved in the determination and differentiation of jaw-closer
muscles in different species will greatly advance our understanding of the
special role these muscles play in evolutionary biology.
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Acknowledgments |
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