Abstract
At the time of the Cold Spring Harbor muscle meeting in 1972 there was much euphoria and great enthusiasm. Essentially all of the investigators there accepted the sliding filament, attached cross-bridge, model of muscle contraction as dogma and many even felt that the problem was solved. Throughout the 1970s and beyond experiments in the muscle field were designed with the underlying assumption of the correctness of the proposed model. After all there was Huxley’s (1969) swinging-tilting cross-bridge model of muscle contraction based on electron microscopic and X-ray diffraction evidence, the transient kinetic mechanical studies of Huxley and Simmons (1971) and the natural way that ATP was proposed to fit into the cross-bridge cycle by Lymn and Taylor (1971). The sliding filament model even appeared in introductory textbooks of physiology. Nonetheless there were difficult but essential issues that had to be addressed. Could the kinetic data derived from the biochemical studies of the actomyosin ATPase reaction mechanism be applied to contracting muscle fibers? Furthermore Huxley (1973) issued a cautionary note at the Cold Spring Harbor meeting when he said that “there is a large gap in our present knowledge, unfortunately right at the heart of the whole problem.” The gap concerned the lack of structural evidence for the proposed changes in the angle of cross-bridge attachment to actin during muscle contraction. This was a enormous problem that would hold up progress in much of the muscle field throughout the 1970s and early 1980s. In fact looking back on this period Huxley (1996) has commented that “…by the mid-1980s, confidence in a straightforward sliding filament mechanism for muscle contraction had been significantly eroded…”. What happened? Why was there skepticism about the sliding filament mechanism of contraction? Between the stagnant 1980s and early twenty-first century there was a spectacular revolution in muscle research that could not have been predicted by even the most ardent dreamer. The investigation of the mechanism of contraction moved from the study of the behavior of billions of cross-bridges in muscle fibers to the investigation of the mechanical properties of individual molecular motors. This work combined with the elucidation of the atomic structures of actin and myosin and the advent of mutagenesis approaches supercharged what would now be called the motility field. But it was still a major challenge to elucidate the mechanism of action of cross-bridges in muscle fibers. In 2004, Hugh Huxley finally proclaimed (Huxley 2004): “…I really do believe that, altogether, there is now incontrovertible evidence for the correctness of the tilting lever-arm model, although of course many important details still remain to be worked out.” (Huxley 2004. With permission John Wiley & Sons Inc) What was the incontrovertible evidence? Was the mechanism of muscle contraction finally solved? These and other issues will be considered in this chapter.
…by the mid-l980s, confidence in a straightforward sliding filament mechanism for muscle contraction had been significantly eroded… (Huxley 1996. With permission Annual Reviews)
H. E. Huxley (1996)
The structure of the myosin head, along with the fit to the actomyosin complex, represented an immense breakthrough in the field, which now can be subdivided into pre- and poststructural periods…A second major breakthrough in the field of motility was the development of in vitro measurements of the force and displacement produced by single myosin molecules. (Cooke 2004. With permission Rockefeller University Press)
R. Cooke (2004)
The main complication is that the action of cross-bridges is never truly synchronized, so what is observed comes from the overlapping cycles of many cross-bridges working in parallel. (Simmons 1992. With permission Elsevier)
R. M. Simmons (1992)
…I really do believe that, altogether, there is now incontrovertible evidence for the correctness of the tilting lever-arm model, although of course many important details still remain to be worked out. (Huxley 2004. With permission John Wiley & Sons Inc.)
H. E. Huxley (2004)
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Notes
- 1.
Some other caged compounds besides caged ATP and caged Pi utilized in muscle research include: caged ADP, caged AMP, caged ATPγS, caged IP3, caged calcium (DM-nitrophen and nitre-5), caged calcium chelators (caged BAPTA and diazo-2) (Homsher and Millar 1990). A variety of biophysical signals, including mechanical, biochemical and structural changes, have been recorded with photolysis of caged compounds (Dantzig et al. 1998).
- 2.
Manuel Francisco Morales (1919–2009) was a strong supporter of Japanese muscle biochemists. He was one of a small number of scientists, including John Gergely, from the United States who attended the first international conference on the chemistry of muscular contraction held in Japan in 1957. For his many contributions to Japanese science, he received the Order of the Rising Sun in Japan in 1989. He was elected to membership in the National Academy of Sciences in 1975. His publications span 66 years with his last publication at 88 years old. (Cooke and Highsmith 2011)
- 3.
It was not possible to record an EPR spectrum during a mechanical transient in the early 1980s. The EPR technique required data collection of 1 min or more and thus was limited to steady states: rigor, rest, steady contraction. Fluorescence polarization (Irving et al. 1995) and the intrinsic technique of birefringence changes (Irving 1993) (See Chap. 1, footnote number 2 and associated text) do have the required sensitivity and temporal resolution.
- 4.
- 5.
Michael P. Sheetz shared the 2012 Lasker award for Basic Medical Research with James A. Spudich and Ronald D. Vale “for discoveries concerning cytoskeletal motor proteins, machines that move cargoes within cells, contract muscles, and enable cell movements.”
- 6.
For a movie from the work of Kron and Spudich (1986) that shows fluorescently labeled actin filaments sliding over muscle myosin molecules that are attached to a glass microscope slide see: http://www.laskerfoundation.org/awards/2012_b_action02.htm.
- 7.
Arthur Ashkin (1922–) is considered by many to be the father of optical trapping using lasers. He received a Ph.D. in physics from Cornell University in 1952 and spent his forty year research career with Bell Laboratories, retiring in 1992. He has received numerous honors and awards and was elected to membership of the National Academy of Sciences in 1996. He has written an overview of the history of the whole field of optical trapping from physics to biology and has complied a compendium of historically significant reprints with commentaries (Ashkin 2006).
- 8.
This work was greatly facilitated by the utilization of video-enhanced differential interference contrast microscopy (VE-DIC) to visualize the moving microtubules. VE-DIC was discovered independently by Robert Allen and colleagues (Allen, Allen, and Travis 1981) and Shinya Inoue (1981). An explanation of the development of the technique and its role in discovering the function of the kinesin motor has been reviewed by Edward D. Salmon (1995). With VE-DIC microscopy it is possible to visualize movement of organelles and macromolecular complexes like microtubules whose dimensions are smaller than the diffraction limit of resolution of the light microscope.
- 9.
- 10.
The numbering of some of the myosin surface loops is approximate since they vary in position slightly and length amongst the various myosin molecules.
- 11.
Fluorescence polarization ratios (Q or sometimes P) are defined as Q⊥ = (⊥I⊥- ║I⊥)/(⊥I⊥ + ║I⊥) and Q║ = (║I║ - ⊥I║)/(║I║ + ⊥I║). The pre- and post-subscripts in the fluorescence intensities (I) indicate excitation (pre) and emission (post) polarization relative to the fiber axis, either perpendicular (⊥) or parallel (║).
- 12.
In X-ray diffraction experiments with whole muscles, an X-ray detector collects information from about 100 muscle fibers (Huxley et al. 2006). Thus single fiber experiments result in an approximate 100 fold lower X-ray detection for the same beam intensity and require extensive signal averaging of repeated contractions. (Reconditi et al. 2004). Nonetheless experiments with single fibers allow almost an order of magnitude higher temporal resolution of mechanical and structural changes than possible with whole muscle. Because muscle fibers diffract X-rays very weakly, it is necessary to use a very bright X-ray source and this means that the experiments must be performed at a synchrotron or electron storage ring facility such as the European Synchrotron Radiation Facility (ESRF), Grenoble, France or the Advanced Photon Source (APS), Argonne National Laboratory (ANL), outside of Chicago, Illinois. (Reconditi et al. 2004; Huxley et al. 2006).
- 13.
One would not expect to see interference effects in the myosin pattern between one A-band in a myofibril and the next A-band in the same myofibril since the actin filaments between them have a subunit repeat different from that of the myosin, and are unlikely to maintain exact registration (Huxley et al. 2006).
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Rall, J.A. (2014). Molecular Mechanism of Force Production: From the Difficult 1980s to the Supercharged 1990s and Beyond. In: Mechanism of Muscular Contraction. Perspectives in Physiology. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2007-5_9
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