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First published online November 2, 2007
Journal of Experimental Biology 210, 3879-3881 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001339
JEB Classics |
THE FIRST DESCRIPTION OF RESILIN
University of Oxford henry.bennet-clark{at}zoo.ox.ac.uk
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). He also
showed that these structures could be strained for weeks without plastic
deformation and, by simple tests, that the elasticity was rubber-like. This
was in contrast to commercial rubbers which are polymeric unsaturated
hydrocarbons: resilin is a cuticular protein that, typically, is deposited
after ecdysis. Weis-Fogh commented on the ability of resilin structures to
snap back after deformation but showed that their rubbery nature was affected
by their hydration and pH. He described a simple test to identify resilin:
with very dilute solutions of Methylene Blue or Toluidine Blue, the protein
stains a deep sapphire blue (Fig.
1B).
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) found resilin
in the salivary pump of assassin bugs, used by the bugs to inject their very
potent mixture of proteolytic enzymes into their prey or, as a defense, to
spit at or inject into aggressors. At around this time, I too found resilin in
the feeding pump of Rhodnius prolixus
(Bennet-Clark, 1963). In both
these examples, the resilin provided an elastic spring antagonist to muscle.
Since then, resilin has bobbed up all over the place. With Eric Lucey, I
described it as the spring that powered the high-speed catapult used in the
flea jumping (Bennet-Clark and Lucey,
1967). More recently, resilin has been described in the amazingly
complex wing-folding mechanism of earwigs (Dermaptera), which tuck away quite
large and fully functional hindwings under tiny, hard forewings
(Haas et al., 2000).
In a later paper on resilin in 1962, Jensen and Weis-Fogh explored its
unique mechanical properties, showing that the energy loss, even at 200 Hz,
was under 5% (Jensen and Weis-Fogh,
1962). They commented that the loss factor does not appear to
increase linearly with frequency, suggesting that the losses are not due to
viscous damping. The context in which Weis-Fogh discussed the dynamic
properties of resilin was the comparatively slow wing-beat frequencies of
locusts (c. 25 Hz) but it has become clear that resilin can act as a useful
spring over far more rapid stress–release cycles. For example, in the
flea Spilopsyllus cuniculi, the catapult releases in less than 1 ms
(Bennet-Clark and Lucey, 1967)
and in cicadas, where resilin acts as the elastic element in the
sound-producing tymbal mechanism (Fig.
1) (Young and Bennet-Clark,
1995), the damped resonant vibration of the tymbal equates with
energy losses in the whole system of under 20%
(Bennet-Clark, 1997). One small
cicada with largely similar resilin-containing tymbals produces sharply
resonant sound pulses at over 13 kHz
(Fonseca and Bennet-Clark,
1998). Thus resilin can work as a useful spring over the very wide
range of speeds encountered in insect biomechanics.
Weis-Fogh had originally found that resilin, almost uniquely among
biological materials, shows perfect elasticity: even when strained to over
twice its original length for two weeks, a dragonfly's resilin tendon snaps
back perfectly when the stress is relieved (hence the name he gave it) and
that it showed neither tearing nor fatigue when stressed within its natural
limits (Weis-Fogh, 1960). He
pointed out that resilin was an ideal material for making elastic joints, such
as hinges, that were subjected to repeated cyclical stress. Yes, indeed: in
the course of its adult life, a locust may fly for 8 hours per day for about
30 days, requiring over 20 million wing beats; a cicada, singing at 4 kHz for
2 or 3 hours per day for more than 20 days, stresses the resilin in each
tymbal over 400 million times, which is more than the number of cycles per
year encountered by the hairspring of a mechanical watch.
Weis-Fogh was never one for hyperbole but, had he been, he would have been
entitled to term resilin a `wonder' material. In his 1960 paper he showed,
with typical economy and elegance, that it was a protein. Its structure and
properties remained unaffected by deep-freezing and heating to over 125°C
and it was unaffected by alcohols and fixatives such as formalin and Bouin's
Solution. However, it was rapidly dissolved by pepsin, trypsin and other
proteolytic enzymes and also dissolved in alkaline solutions; this last snag
may partly explain why Snodgrass
(Snodgrass, 1946) shows gaps
in the meta-pleural regions of fleas whereas I, using freshly killed fleas,
observed that these regions stained brilliantly with Methylene Blue
(Bennet-Clark and Lucey, 1967).
The disappearance of resilin in the course of routine preparation of insect
exoskeletons may also partly explain why it remained undetected for so long,
but I prefer to think that Weis-Fogh knew that there must be some interesting
elastic elements in insects and set out to search for them.
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). Dityrosine
fluoresces in UV light, being maximally excited with light at 315 nm and
radiating maximally at 430 nm (Andersen and
Weis-Fogh, 1964; Elvin et al.,
2005): this provides a useful way of identifying resilin
non-invasively (see Fig.
1C).
What does the future hold? Chris Elvin and his colleagues, working in
Australia (Elvin et al., 2005)
have successfully inserted the gene for pro-resilin into Escherichia
coli, obtaining the gene product and then cross-linking this product and
casting it into quite large structures
(Fig. 2) with remarkably high
resilience: in other words, they've been able to produce resilin in
potentially useful quantities and with the potential to form it into
structures. Elvin suggests that applications could range from spinal disc
implants and heart and blood valve substitutes to high-efficiency industrial
rubbers, microactuators and nanosprings. There are serious practical problems
to overcome, however, the most serious of which appear to be the ease with
which resilin can be de-natured by proteases, the effects of pH and hydration
on its mechanical properties and, in the context of a prosthesis, that it
could create an immune response.
Nevertheless, the amazing properties of resilin will encourage further development of solutions to practical problems.
Footnotes
Henry Bennet-Clark writes about Torkel Weis-Fogh's classic paper on resilin entitled `A rubber-like protein in insect cuticle'. A copy of the paper can be obtained at http://jeb.biologists.org/cgi/reprint/37/4/889.
References
Andersen, S. O. (1964). The cross links in resilin identified as dityrosine and trityrosine. Biochim. Biophys. Acta 93,213 -215.[Medline]
Andersen, S. O. and Weis-Fogh, T. (1964). Resilin. A rubber-like protein in arthropod cuticle. Adv. Insect Physiol. 2,1 -65.
Bennet-Clark, H. C. (1963). Negative pressures produced in the pharyngeal pump of the bloodsucking bug, Rhodnius prolixus. J. Exp. Biol. 40,223 -229.[Abstract]
Bennet-Clark, H. C. (1997). Tymbal mechanics and the control of song frequency in the cicada Cyclochila australasiae.J. Exp. Biol. 200,1681 -1694.[Abstract]
Bennet-Clark, H. C. and Lucey, E. C. A. (1967).
The jump of the flea: a study of the energetics and a model of the mechanism.
J. Exp. Biol. 47,59
-76.
Edwards, J. S. (1960). Predation and digestion in assassin bugs (Heteroptera, Reduviidae). PhD thesis, University of Cambridge, UK.
Elvin, C. M., Carr, A. G., Huson, M. G., Maxwell, J. M., Pearson, R. D., Vuocolo, T., Liyou, N. E., Wong, D. C. C., Merritt, D. J. and Dixon, N. E. (2005). Synthesis and properties of crosslinked recombinant pro-resilin. Nature 437,999 -1002.[CrossRef][Medline]
Fonseca, P. J. and Bennet-Clark, H. C. (1998). Asymmetry of tymbal action and structure in a cicada: a possible role in the production of complex songs. J. Exp. Biol. 201,717 -730.[Medline]
Haas, F., Gorb, S. and Wootton, R. J. (2000). Elastic joints in dermapteran hind wings: materials and wing folding. Arthropod Struct. Develop. 29,137 -146.[CrossRef]
Jensen, M. and Weis-Fogh, T. (1962). Biology and physics of locust flight. V. Strength and elasticity of locust cuticle. Phil. Trans. Roy. Soc. Lond. B 245,137 -169.[CrossRef]
Snodgrass, R. E. (1946). The skeletal anatomy of fleas. Smithsonian Miscellaneous Collections 104, 1-89.
Weis-Fogh, T. (1960). A rubber-like protein in insect cuticle. J. Exp. Biol. 37,889 -907.[Abstract]
Young, D. and Bennet-Clark, H. C. (1995). The role of the tymbal in cicada sound production. J. Exp. Biol. 198,1001 -1019.[Medline]
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