Do muscles function as adaptable locomotor springs?
1 Physiology and Functional Morphology Group, Department of Biological
Sciences, Northern Arizona University, Flagstaff, AZ 86011-5640,
USA
2 Department of Physical Therapy, Northern Arizona University, Flagstaff, AZ
86011-5640, USA
* e-mail: Stan.Lindstedt{at}nau.edu
Accepted 13 May 2002
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Summary |
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Key words: elastic recoil, strain energy, eccentric, hopping, stride frequency, titin, muscle
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Usual view of muscle |
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However, whenever the opposing force acting on a muscle exceeds the force
produced by the muscle, the muscle will lengthen while being activated,
absorbing mechanical work. The past few decades have brought an increased
understanding of the importance of these lengthening (eccentric) contractions
in normal animal movement. While the obvious examples include hiking downhill
or cushioning a fall, recent evidence implicates eccentric contractions as an
integral part of most cyclic movements, especially in terrestrial locomotion.
For example, many locomotor muscles are actively stretched prior to
shortening, described as the stretchshorten cycle
(Komi and Bosco, 1978;
Hof et al., 1983
;
Ettema, 1996b
). Whenever work
is done on a muscle, or muscle/tendon element, energy is absorbed. This
absorbed energy can either be lost as heat (as it is when hiking downhill) or
stored as elastic strain energy (elastic recoil potential energy), a portion
of which may subsequently be recovered
(Asmussen and Bonde-Petersen
1974
; Komi and Bosco,
1978
; Biewener and Roberts,
2000
; Ettema,
1996b
; Dickinson et al.,
2000
; Lindstedt et al.,
2001
). The storage and recovery of elastic strain energy may be of
greatest `energetic value' when locomotor muscles perform a
stretchshorten cycle because the energy stored during a lengthening
cycle can amplify force production in a subsequent shortening cycle
(Komi and Bosco, 1978
;
Biewener and Roberts, 2000
;
Ettema et al., 1990
;
Prilutsky et al., 1996
;
Olson and Marsh, 1998
;
Seyfarth et al., 2000
). The
pervasive role of eccentric muscular force may be most substantial during
highforce locomotor movements such as running
(Cavagna et al., 1971
;
Cavagna, 1977
), sprinting
(Mero and Komi, 1986
;
Farley, 1997
;
Chelly and Denis, 2001
),
hopping (Chelly and Denis,
2001
; Lindstedt et al.,
2001
) and jumping (Seyfarth et
al., 2000
). Here, we examine how these kinds of muscle uses can be
quantified and ask if there is evidence that muscle may adapt to eccentric
contractions.
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Lengthening contractions in normal locomotion |
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However, while tendons certainly function to store strain energy, their
relative contribution is apparently greatest in animals with long tendons,
such as turkeys, and in large animals
(Pollock and Shadwick, 1994;
Ettema, 1996a
). The tendons of
small animals are not proportioned to optimize this function
(Bennett and Taylor, 1995
),
although small animals can still recover some elastic strain energy during
locomotion (Ettema, 1996a
).
This ability to recover elastic strain energy is apparently energetically so
advantageous that stride frequency in running mammals may be set by this key
property alone (Taylor, 1985
;
Farley et al., 1993
). In
addition, ample evidence shows that storage and recovery of elastic strain
energy can occur in the absence of tendons
(Cavagna et al., 1994
). Thus,
apart from the role of tendons and collagen in energy storage, the muscle
itself is certainly contributing to the storage and recovery of elastic strain
energy. In a sense, because the muscle is composed of both muscle fibers and
tendinous materials, all these structures must be collectively `tuned' to the
spring properties for the muscle/tendon system to store and recover elastic
strain energy during locomotion.
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Elastic strain energy storage in muscle itself |
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How does the muscle spring adapt to eccentric contractions? |
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One dramatic anecdotal example suggests that the answer is yes. If
naïve to hiking downhill (eccentric lengthening contractions), one can
experience devastating delayed onset muscle soreness (DOMS) after an initial
hike (Armstrong, 1984). There
is strong evidence linking DOMS with muscle damage, suggesting that the muscle
cells themselves have been injured. For example, levels of the myoplasm enzyme
creatine kinase may increase to concentrations two orders of magnitude higher
in the blood after acute eccentric exercise
(Bar et al., 1997
), indicative
of serious muscle damage. Likewise, structural damage to the contractile
elements of the muscle fiber can be seen directly by electron microscopy. The
most frequent observation is Z-band streaming
(Friden et al., 1983
;
Bar et al., 1997
). However, if
one hikes downhill repeatedly, after relatively few hikes there is no soreness
or muscle damage whatsoever. Hence, the chronic use of eccentric contractions,
in this case downhill hiking, results in a pronounced protective adaptation
termed the `repeated bout effect'
(Clarkson and Tremblay, 1988
;
Ebbeling and Clarkson, 1990
;
Nosaka et al., 1991
) within
the muscle. In fact, this protective adaptation occurs between 48 and 72 h
after the initial exercise (Nosaka and
Clarkson, 1996
; Smith et al.,
1994
) and may be evident as soon as 24h after a first damaging
eccentric bout (Chen and Hsieh,
2001
). Consequently, the identical eccentric activity that caused
serious damage no longer has any harmful effect.
What is the nature of this adaptation? The changes within the muscle
responsible for this adaptation are largely unknown. There are, however,
suggestions that groups of the more fragile, stress-susceptible fibers are
reduced in number after the first bout while stronger fibers survive and
provide a protective effect (Armstrong,
1984). Even light eccentric training protocols, however, that do
not lead to an increase in creatine kinase levels and do little or no muscle
damage, are still sufficient to bring about protection
(Clarkson and Tremblay, 1988
).
It is also possible that the protective effect may lie outside the muscle and
is neurologically mediated, i.e. that muscle fibers specifically adapted to
repeated eccentric contractions may be preferentially recruited
(Golden and Dudley, 1992
;
Hortobagyi et al., 1996
).
Hence, while the exact nature of this adaptation is as yet unknown, one
possibility remains that the muscle/tendon structure may become functionally
`stiffer', allowing the muscle to absorb mechanical work without damage. Some
have reported that training produces a less compliant locomotor muscle
(Benn et al., 1998
;
Pousson et al., 1990
;
Reich et al., 2000
), while
others note greater elastic recoil in trained compared with untrained subjects
(Kubo et al., 2000
).
To investigate further the hypothesis of muscle/tendon stiffness
plasticity, we used two model systems which both suggest that muscle `spring
stiffness' can indeed change acutely in response to chronic eccentric muscle
use. Young, healthy human subjects rode a high-force eccentric ergometer for 8
weeks (30 min three times per week). The eccentric load was gradually
increased in these subjects until, during the final 3 weeks, subjects were
working at nearly -500 W (i.e. absorbed power) (see
LaStayo et al., 2000). While
this training resulted in increased muscle strength and size
(LaStayo et al., 2000
), we
were also interested in how it affected the apparent muscle spring stiffness.
To investigate the impact of this high-force eccentric training on
muscle/tendon stiffness, we performed two experiments. In the first, the
subjects hopped `in place' vertically with instructions to select the
frequency that felt the most comfortable. The subjects performed successive
counter-measure hops to a height equal to 107% of subject height. We regularly
use this as a physiology laboratory exercise because it demonstrates how the
`comfortable frequency' is the most economical; the cost per hop doubles when
the subjects are forced to hop at half this frequency (see
Lindstedt et al., 2001
).
Following eccentric training, all the subjects selected a higher hopping
frequency than they did prior to training; the 12% mean overall increase was
highly significant, while none of the control subjects (those exercising on a
traditional, concentric bicycle) changed their hopping frequency
(Fig. 1).
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Another set of subjects (local high school basketball players) were trained
with the same protocol. In this case, we recorded their maximum (vertical)
jump height before and after 6 weeks of high-force eccentric cycle ergometry
training. A weight-training control group was drawn from the same high school
basketball players. Maximum jump height was taken as the peak of three jumps.
While both groups of subjects had identical initial maximum jump heights at
the start of the study, all the eccentric-trained subjects increased their
jump height, with the overall mean increase being approximately 8%
(approximately 5 cm, Fig. 2).
Thus, not only does high-force eccentric training evoke gains in muscle
strength (Hortobagyi et al.,
1996; LaStayo et al.,
1999
,
2000
) and size
(Hortobagyi et al., 1996
;
LaStayo et al., 2000
), it
apparently also results in a significant increase in the muscle spring
stiffness (Lindstedt et al.,
2001
). In response to high-force eccentric training, hopping
frequency increased and subjects were able to jump significantly higher,
suggesting an enhanced strain energy storage and recovery when performing
single or repeated counter-measure jumps (see also
Seyfarth et al., 2000
).
|
To examine whether this apparent increased stiffness was a result of
changes in the muscle contractile properties, we used a model of rats walking
down a steep (36%) decline. To ensure eccentric loading, we added an
additional weight equal to 15% of body mass to small Velcro backpacks. After 8
weeks of running (30 min five times per week), the triceps muscles of the
eccentrically trained animals were significantly stiffer than those of the
inactive controls (Reich et al.,
2000). These in vitro measurements of active muscle
stiffness excluded that portion of tendon outside the muscle belly and, hence,
reflect muscle belly stiffness. The point is that, after just 8 weeks of
training, the muscle had indeed demonstrated a structural adaptation by
becoming approximately 40% `stiffer', without an increase in either muscle
mass or isometric force production capabilities, when subjected to chronic
eccentric use. Thus, we conclude that the apparent increases in muscle/tendon
stiffness in the human subjects were also probably attributable primarily to
shifts in muscle stiffness.
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Where and what is the muscle spring? |
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Titin, the third filament system within muscles, is thought to be
responsible for the elastic properties of vertebrate myofibrils. Discovered
over two decades ago (Maruyama et al.,
1977), titin is a huge protein (2.5-3.5 MDa), and is the only
known protein to span an entire half-sarcomere from Z-disc to M-line with
cross-links from titin molecules of adjacent sarcomeres in both regions
(Obermann et al., 1997
) (for a
review, see Gregorio et al.,
1999
). The I-band region of titin functions as a molecular spring
that develops tension when sarcomeres are stretched (Linke et al.,
1996
,
1999
;
Linke and Granzier, 1998
).
This force is responsible for restoring the muscle to slack length after being
stretched beyond or shortened below resting length
(Helmes et al., 1996
) and for
maintaining the structural integrity of the sarcomere in actively contracting
muscle (Horowits and Podolsky,
1987
). Because titin has numerous binding sites for other proteins
within the sarcomere, it is likely that it provides a blueprint for precise
sarcomere assembly (Gregorio et al.,
1999
; van der Ven et al.,
2000
).
Although there is only one titin gene, there are multiple titin isoforms
which vary in I-band region stiffness. These isoforms vary in their lengths of
serially linked immunoglobulin-like domains (Ig domains) and lengths of a
region rich in proline (P), glutamate (E), valine (V) and lysine (K) residues
(PEVK region) because of an uncharacterized, complicated method of
differential splicing (Labeit and
Kolmerer, 1995; Centner et
al., 2000
). Passive tension/stiffness properties of skeletal
muscle tissues differ; for example, cardiac cells are much stiffer than
skeletal muscle cells. These differences in stiffness/passive tension
properties correspond to differences in titin isoform expression because
titins from different tissues have different electrophoretic mobilities
(Wang et al., 1991
;
Frieburg et al., 2000
).
Because of these structural properties, titin could play a significant role
as the muscle spring, which could explain why titin isoforms differ in
skeletal tissues. For example, it is thought to play a key function in cardiac
contractility, having been called the `missing link' of diastole since it may
contribute significantly to the FrankStarling law of the heart
(LeWinter, 2000). Second, as a
muscle-stiffening spring, it may play a key role in the protective effect that
occurs following eccentric exercise (Reich
et al., 2000
). Supporting this idea is the fact that high-force
eccentric damage includes `titin failure'
(Thompson et al., 1999
).
Finally, in addition to all titin's known functions, the titin filament system
may play a dynamic functional role in muscle contraction. Labeit and Kolmerer
(1995
) identified strong
negative charges in the PEVK regions, which provide potential
Ca2+-binding sites. It has recently been shown that titin has an
affinity for calcium in the 5'-most 400 kDa region of the PEVK segment
(Tatsumi et al., 2001
). With
the binding of Ca2+, the secondary structure of this titin fragment
changes (Tatsumi et al.,
2001
). Thus, it has been speculated that the elasticity of titin
changes in response to the flux of Ca2+ within the sarcomere during
contraction/relaxation cycling (Tatsumi et
al., 2001
). It has also been suggested that the differential
expression of titin isoforms mediates active force production by influencing
the sensitivity of the myofilaments to activation by Ca2+
(Cazorla et al., 2001
), by
mediating changes in interfilament spacing
(Cazorla et al., 2001
) and by
inducing conformational changes in myosin that result in a higher probability
of activation at a given Ca2+ concentration
(Fukuda et al., 2001
;
Granzier and Wang, 1993a
).
Thus, the differential expression of titin isoforms may in fact provide the
means for the dynamic regulation of active force production
(Sutko et al., 2001
).
If titin is functioning as a locomotor spring, then it should be `tuned' to
the frequency of muscle use. One way we can we can test this hypothesis is to
examine titin isoforms in muscles that are used cyclically at different
frequencies. Because stride frequency varies predictably with body size among
mammals, by examining the titin expressed in differently sized animals we
would detect shifts in titin isoforms as a function of body size. In
particular, stride frequency at the trot/gallop transition (a physiologically
equivalent speed) varies quite predictably as 4.5M-0.14
(r2=0.98, where M is body mass)
(Heglund et al., 1974). Thus,
comparing the predicted stride frequency of a 25 g mouse with that of a 800 kg
cow, stride frequency should decline from a predicted 7.5 to 1.8
s-1. Since the muscle spring is highly time-dependent
(Cavagna et al., 1994
), if
titin were to play a role in the storage and recovery of elastic strain
energy, it should be much stiffer in a mouse than in a cow, reflecting the
4.3-fold difference in frequencies.
To examine this possibility, we identified the titin isoform present by
electrophoresis using SDS-PAGE following and modifying the techniques of
Granzier and Wang (1993b) and
Granzier and Irving (1995
).
Vastus lateralis from mouse, rabbit, dog and calf were quick-frozen in liquid
nitrogen. The samples were pulverized and the proteins extracted in Laemmli's
sample buffer. The samples were analyzed with SDS-PAGE (4% to 10% acrylamide
gradient gels). The gels were run at 5.5 mA and 12°C for 22 h. After
electrophoretic separation, the gels were stained with Coomassie Blue. The
stained gels were scanned at 600 d.p.i. using a snap scan 1212 (AGFA) flatbed
scanner. Within each lane, nebulin (780 kDa) acted as a standard. With the
naked eye, it is apparent that at least two isoforms are expressed in these
animals and that there is a significant and predictable shift from the most
compliant (largest) isoforms in the cow to the stiffest (and smallest)
isoforms in the mouse (Fig. 3).
Thus, the results of these gels suggest a strong link between stride frequency
and titin `stiffness'. While this does not by itself demonstrate that titin is
the muscle spring, it certainly suggests that it may be a significant and
potentially `tuned' contributor to the muscle/tendon `tuned' spring.
|
In the future, we plan to investigate this final idea in detail by examining the titin isoforms present in a wide variety of mammalian muscles functioning cyclically, including the heart, the diaphragm and other locomotor muscles.
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Acknowledgments |
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References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alexander, R. McN. and Bennet-Clark, H. C. (1977). Storage of elastic strain energy in muscle and other tissues. Nature 265,114 -117.[Medline]
Armstrong, R. B. (1984). Mechanisms of exercise-induced delayed onset muscular soreness: a brief review. Med. Sci. Sport Exerc. 16,529 -538.[Medline]
Asmussen, E. and Bonde-Petersen, F. (1974). Apparent efficiency and storage of elastic energy in humans during exercise. Acta Physiol. Scand. 92,537 -545[Medline]
Bar, P. R., Reijneveld, J. C., Wokke, J., Jacobs, C. J. M. and Bootsma, A. (1997). Muscle damage induced by exercise: nature, prevention and repair. In Muscle Damage (ed. S. Salmons), pp. 1-27. Oxford: Oxford University Press.
Benn, C., Forman, K., Mathewson, D., Tapply, M., Tiskus, S., Whang, K. and Blanpied, P. (1998). The effects of serial stretch loading on stretch work and stretchshorten cycle performance in the knee musculature. J. Orthop. Sport Phys. Ther. 6, 412-422.
Bennett, M. B. and Taylor, G. C. (1995). Scaling of elastic strain energy in kangaroos and the benefits of being big. Nature 378,56 -59.[Medline]
Biewener, A. A. and Blickhan, R. (1988). Kangaroo rat locomotion: design for elastic energy storage or acceleration? J. Exp. Biol. 140,243 -255.[Abstract]
Biewener, A. A. and Roberts, T. J. (2000). Muscle and tendon contributions to force, work and elastic energy savings: A comparative perspective. Exerc. Sports Sci. Rev. 28, 99-107.
Booth, F. W. and Baldwin, K. M. (1996). Muscle plasticity: energy demand and supply processes. In Handbook of Physiology, section 12, Exercise: Regulation and Integration of Multiple Systems (ed. L. B. Rowell and J. T. Shepherd), pp.1075 -1123. New York: Oxford University Press.
Bosco, C., Tihanyi, J., Komi, P. V., Fekete, G. and Apor, P. (1982). Store and recoil of elastic energy in slow and fast types of human skeletal muscles. Acta Physiol. Scand. 116,343 -349.[Medline]
Cavagna, G. A. (1977). Storage and utilization of elastic energy in skeletal muscle. Exerc. Sports Sci. Rev. 5,9 -129.
Cavagna, G. A., Heglund, N. C., Harry, J. D. and Mantovani, M. (1994). Storage and release of mechanical energy by contracting frog muscle fibres. J. Physiol., Lond. 481,689 -708.[Abstract]
Cavagna, G. A., Komarek, L. and Mazzoleni, S. (1971). The mechanics of sprint running. J. Physiol., Lond. 217,709 -721.[Medline]
Cavagna, G. A., Mazzanti, M., Heglund, N. C. and Citteris, G. (1985). Storage and release of mechanical energy by active mucle: a non-elastic mechanism? J. Exp. Biol. 115, 79-87.[Abstract]
Cazorla, O., Wu, Y., Irving, T. C. and Granzier, H.
(2001). Titin-based modulation of calcium sensitivity of active
tension in mouse skinned cardiac myocytes. Circ. Res.
88,1028
-1035.
Centner, T., Fougerousse, F., Freiburg, A., Witt, C., Beckmann, J. S., Granzier, H., Trombitas, K., Gregorio, C. C. and Labeit, S. (2000). Molecular tools for the study of titin's differential expression. Elastic Fil. Cell 481, 35-49.
Chelly, S. M. and Denis, C. (2001). Leg power and hopping stiffness: relationship with sprint running performance. Med. Sci. Sport Exerc. 2, 326-333.
Chen, T. C. and Hsieh, S. S. (2001). Effects of 7-day eccentric training period on muscle damage and inflammation. Med. Sci. Sport Exerc. 33,1732 -1738.[Medline]
Clarkson, P. M. and Tremblay, I. (1988). Rapid
adaptation to exercise-induced muscle damage. J. Appl.
Physiol. 65,1
-6.
Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, A. R.,
Kramm, R. and Lehman, S. (2000). How animals move: an
integrative view. Science
288,100
-106.
Ebbeling, C. B. and Clarkson, P. M. (1990). Muscle adaptation prior to recovery following eccentric exercise. Eur. J. Appl. Physiol. 60, 26-31.
Ettema, G. J. C. (1996a). Elastic and
lengthforce characteristics of the gastrocnemius of the hopping mouse
(Notomys alexis) and the rat (Rattus norvegicus).
J. Exp. Biol. 199,1277
-1285.
Ettema, G. J. C. (1996b). Mechanical efficiency
and efficiency of storage and release of series elastic energy in skeletal
muscle during stretchshorten cycles. J. Exp.
Biol. 199,1983
-1997.
Ettema, G. C., Huijing, P. A., van Ingen Schenau, G. J. and de Haan, A. (1990). Effects of prestretch at the onset of stimulation on mechanical work output of rat medial gastrocnemius muscletendon complex. J. Exp. Biol. 152,333 -351.[Abstract]
Farley, C. T. (1997). Maximum speed and
mechanical power output in lizards. J. Exp. Biol.
200,2189
-2195.
Farley, C. T., Glasheen, J. and McMahon, T. A.
(1993). Running springs: speed and animal size. J.
Exp. Biol. 185,71
-86.
Friden, J., Sjostrom, M. and Ekblom, B. (1983). Myofibrillar damage following intense eccentric exercise in man. Int. J. Sports Med. 4,170 -176.[Medline]
Frieburg, A., Trombitas, K., Hell, W., Cazorla, O., Fougerousse,
F., Centner, T., Kolmerer, B., Witt, C., Beckmann, J. S., Gregorio, C. C.,
Granzier, H. and Labeit, S. (2000). Series of exon-skipping
events in the elastic spring region of titin as the structural basis for
myofibrillar elastic diversity. Circ. Res.
86,1114
-1121.
Fukuda, N., Sasaki, D., Ishiwata, S. and Kurihara, S.
(2001). Length dependence of tension generation in rat skinned
cardiac muscle: role of titin in the Frank Starling mechanism of the heart.
Circulation 104,1639
-1645.
Golden, C. and Dudley, G. A. (1992). Strength after bouts of eccentric or concentric actions. Med. Sci. Sport Exerc. 24,926 -933.[Medline]
Granzier, H. L. M. and Irving, T. C. (1995). Passive tension in cardiac muscle: contribution of collagen, titin, microtubules and intermediate filaments. Biophys. J. 68,1027 -1044.[Abstract]
Granzier, H. L. M. and Wang, K. (1993a). Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filaments. Biophys. J. 65,2141 -2159.[Abstract]
Granzier, H. L. M. and Wang, K. (1993b). Gel electrophoresis of giant proteins: Solubilization and silver-staining of titin and nebulin from single muscle fiber segments. Electrophoresis 14,56 -64.[Medline]
Gregorio, C. C., Granzier, H., Sorimachi, H. and Labeit, S. (1999). Muscle assembly: a titanic achievement? Curr. Opin. Cell Biol. 11,18 -25.[Medline]
Han, X. Y., Wang, W., Komulainen, J., Koskinen, S. O. A., Kovanen, V., Vihko, V., Trackman, P. C. and Takala, T. E. S. (1999). Increased mRNAs for procollagens and key regulating enzymes in rat skeletal muscle following downhill running. Pflügers Arch. 437,857 -864.[Medline]
Heglund, N. C., Taylor, C. R. and McMahon, T. A. (1974). Scaling stride frequency and gait to animal size: Mice to horses. Science 186,1112 -1113.[Medline]
Helmes, M., Trombitas, K. and Granzier, H.
(1996). Titin develops restoring force in rat cardiac myocytes.
Circ. Res. 79,619
-626.
Hof, A. L., Geelen, B. A. and van den Berg, J. W. (1983). Calf muscle moment, work and efficiency in level walking; role of series elasticity. J. Biomech. 25,953 -965.
Horowits, R. and Podolsky, R. J. (1987). The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: Evidence for the role of titin filaments. J. Cell Biol. 105,2217 -2223.[Abstract]
Hortobagyi, T., Hill, J. P., Houmard, J. A., Fraser, D. D.,
Lambert, N. J. and Israel, R. G. (1996). Adaptive responses
to muscle lengthening and shortening in humans. J. Appl.
Physiol. 80,765
-772.
Komi, P. V. and Bosco, C. (1978). Utilization of stored elastic energy in leg extensor muscles by men and women. Med. Sci. Sport Exerc. 10,261 -265.
Kubo, K., Kanehisa, H., Kawakami, Y. and Fukunaga, T. (2000). Elastic properties of muscletendon complex in long-distance runners. Eur. J. Appl. Physiol. 81,181 -187.[Medline]
Labeit, S. and Kolmerer, B. (1995). Titins: Giant proteins in charge of muscle ultrastructure and elasticity. Science 270,293 -296.[Abstract]
LaStayo, P. C., Pierotti, D. J., Pifer, J., Hoppeler, H. and Lindstedt, S. L. (2000). Eccentric ergometry: Increases in locomotor muscle size and strength at low training intensities. Am. J. Physiol. 278,R1282 -R1288.
LaStayo, P. C., Reich, T. E., Urquhart, M., Hoppeler, H. and
Lindstedt, S. L. (1999). Chronic eccentric exercise:
improvements in muscle strength can occur with little demand for oxygen.
Am. J. Physiol. 276,R611
-R615.
Lensel-Corbeil, G. and Goubel, F. (1989). Series elasticity in frog sartorius muscle during release and stretch. Arch. Int. Physiol. Biochem. 97,499 -509.[Medline]
LeWinter, M. M. (2000). Titin: the `missing link' of diastole. J. Mol. Cell. Cardiol. 32,2111 -2114.[Medline]
Lindstedt, S. L., LaStayo, P. C. and Reich, T. E.
(2001). When active muscles lengthen: properties and consequences
of eccentric contractions. News Physiol. Sci.
16, 256-261
Linke, W. A. and Granzier, H. (1998). A spring
tale: new facts on titin elasticity. Biophys. J.
75,2613
-2614.
Linke, W. A., Ivemeyer, M., Olivieri, N., Kolmerer, B., Ruegg, J. C. and Labeit, S. (1996). Towards a molecular understanding of the elasticity of titin. J. Mol. Biol. 261,62 -71.[Medline]
Linke, W. A., Rudy, D. E., Centner, T., Gautel, M., Witt, C.,
Labeit, S. and Gregorio, C. C. (1999). I-band titin in
cardiac muscle is a three element molecular spring and is critical for
maintaining thin filament structure. J. Cell Biol.
146,631
-644.
Luthanen, P. and Komi, P. V. (1980). Force, power and elasticityvelocity relationships in walking, running and jumping. Eur. J. Appl. Physiol. 44,279 -289.
Maruyama, K., Matsubara, S., Natori, R., Nonomura, Y., Kimura, S., Ohashi, K., Murakami, F., Handa, S. and Eguchi, G. (1977). Connectin, an elastic protein of muscle: characterization and function. J. Biochem. 82,317 -337.[Medline]
McMahon, T. A. (1984). Muscles, Reflexes and Locomotion. Princeton: Princeton University Press.
Mero, A. and Komi, P. V. (1986). Force, EMG and elasticityvelocity relationships at submaximal, maximal and supramaximal running speeds in sprinters. Eur. J. Appl. Physiol. 55,553 -561.
Nosaka, K. and Clarkson, P. M. (1996). Changes in indicators of inflammation after eccentric exercise of the elbow flexors. Med. Sci. Sport Exerc. 28,953 -961.[Medline]
Nosaka, K., Clarkson, P. M., McGuiggin, M. E. and Byrne, J. M. (1991). Time course of muscle adaptation after high-force eccentric exercise. Eur. J. Appl. Physiol. 63, 70-76.
Obermann, W. M., Gautel, M., Weber, K. and Furst, D. O.
(1997). Molecular structure of the sarcomeric M band: mapping of
titin and myosin binding domains in myomesin and the identification of a
potential regulatory phosphorylation site in myomesin. EMBO
J. 16,211
-220.
Olson, J. M. and Marsh, R. L. (1998).
Activation patterns and length changes in hindlimb muscles of the bullfrog
Rana catesbeiana during jumping. J. Exp.
Biol. 201,2763
-2777.
Pollock, C. M. and Shadwick, R. E. (1994).
Allometry of muscle, tendon and elastic energy storage capacity in mammals.
Am. J. Physiol. 266,R1022
-R1031.
Pousson, M., Van Hoecke, J. and Goubel, F. (1990). Changes in elastic characteristics of human muscle induced by eccentric exercise. J. Biomech. 23,343 -348.[Medline]
Prilutsky, B. I., Herzog, W., Leonard, T. R. and Allinger, T. L. (1996). Role of the muscle belly and the tendon of soleus, gastrocnemius and plantaris in mechanical energy absorption and generation during cat locomotion. J. Biomech. 29,417 -434.[Medline]
Reich, T. E., Lindstedt, S. L., LaStayo, P. C. and Pierotti, D. J. (2000). Are muscle springs plastic? Am. J. Physiol. 278,R1661 -R1666.
Roberts, T. J., Marsh, R. L., Weyland, P. G. and Taylor, C.
R. (1997). Muscular force in running turkeys: The economy of
minimizing work. Science
275,1113
-1115.
Seyfarth, A., Blickhan, R. and Van Leeuwen, J. L.
(2000). Optimal take-off techniques and muscle design for long
jump. J. Exp. Biol. 203,741
-750.
Smith, L. L., Fulmer, M. G., Holbert, D., McCammon, M. R., Houmard, J. A., Frazer, D. D., Nsien, E. and Israel, R. G. (1994). The impact of a repeated bout of eccentric exercise on muscular strength, muscle soreness and creatine kinase. Br. J. Sports Med. 28,267 -271.[Abstract]
Staron, R. S., Leonardi, M. J., Karapondo, D. L., Molicky, E.
S., Folkel, J. E., Hagerman, F. C. and Hikida, R. S. (1991).
Strength and skeletal muscle adaptations in heavy resistance-trained women
after de-training and re-training. J. Appl. Physiol.
70,631
-640.
Sutko, J. L., Publicover, N. G. and Moss, R. L.
(2001). Titin: an elastic link between length and active force
production in myocardium. Circulation
104,1585
-1587.
Tatsumi, R., Maeda, K., Hattori, A. and Takahashi, K. (2001). Calcium binding to an elastic portion of connectin/titin filaments. J. Muscle Res. Cell Motil. 22,149 -162.[Medline]
Taylor, C. R. (1985). Force development during sustained locomotion: a determinant of gait, speed and metabolic power. J. Exp. Biol. 115,253 -262.[Abstract]
Thompson, J. L., Balog, E. M., Fitts, R. H. and Riley, D. A. (1999). Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle a test model. Anat. Rec. 254,39 -52.[Medline]
Tidball, J. G. and Daniel, T. L. (1986). Elastic energy storage in rigored skeletal muscle cells under physiological loading conditions. Am. J. Physiol. 250,R56 -R64.[Medline]
van der Ven, P. F. M., Bartsch, J. W., Gautel, M., Jockusch, H.
and Furst, D. O. (2000). A functional knock-out of titin
results in defective myofibril assembly. J. Cell Sci.
113,1405
-1414.
Wang, K., McCarter, R., Wright, J., Beverly, J. and Ramirez-Mitchell, R. (1991). Regulation of skeletal muscle stiffness and elasticity by titin isoforms: A test of the segmental extension model of resting tension. Proc. Natl. Acad. Sci. USA 88,7101 -7105.[Abstract]
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