Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1998 Aug;75(2):938–947. doi: 10.1016/S0006-3495(98)77582-4

Elastic properties of isolated thick filaments measured by nanofabricated cantilevers.

T Neumann 1, M Fauver 1, G H Pollack 1
PMCID: PMC1299767  PMID: 9675194

Abstract

Using newly developed nanofabricated cantilever force transducers, we have measured the mechanical properties of isolated thick filaments from the anterior byssus retractor muscle of the blue mussel Mytilus edulis and the telson levator muscle of the horseshoe crab Limulus polyphemus. The single thick filament specimen was suspended between the tip of a flexible cantilever and the tip of a stiff reference beam. Axial stress was placed on the filament, which bent the flexible cantilever. Cantilever tips were microscopically imaged onto a photodiode array to extract tip positions, which could be converted into force by using the cantilever stiffness value. Length changes up to 23% initial length (Mytilus) and 66% initial length (Limulus) were fully reversible and took place within the physiological force range. When stretch exceeded two to three times initial length (Mytilus) or five to six times initial length (Limulus), at forces approximately 18 nN and approximately 7 nN, respectively, the filaments broke. Appreciable and reversible strain within the physiological force range implies that thick-filament length changes could play a significant physiological role, at least in invertebrate muscles.

Full Text

The Full Text of this article is available as a PDF (326.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bennett P. M., Elliott A. The 'catch' mechanism in molluscan muscle: an electron microscopy study of freeze-substituted anterior byssus retractor muscle of Mytilus edulis. J Muscle Res Cell Motil. 1989 Aug;10(4):297–311. doi: 10.1007/BF01758426. [DOI] [PubMed] [Google Scholar]
  2. Chick J. J., Stephenson D. G. The effect of temperature on contractile activation of intact and chemically skinned 'catch' muscle fibre bundles of Mytilus edulis. J Muscle Res Cell Motil. 1995 Jun;16(3):285–294. doi: 10.1007/BF00121137. [DOI] [PubMed] [Google Scholar]
  3. Cohen C., Szent-Györgyi A. G., Kendrick-Jones J. Paramyosin and the filaments of molluscan "catch" muscles. I. Paramyosin: structure and assembly. J Mol Biol. 1971 Mar 14;56(2):223–227. doi: 10.1016/0022-2836(71)90461-x. [DOI] [PubMed] [Google Scholar]
  4. DEVILLAFRANCA G. W., MARSCHHAUS C. E. CONTRACTION OF THE A BAND. J Ultrastruct Res. 1963 Aug;49:156–165. doi: 10.1016/s0022-5320(63)80043-x. [DOI] [PubMed] [Google Scholar]
  5. Dewey M. M., Walcott B., Colflesh D. E., Terry H., Levine R. J. Changes in thick filament length in Limulus striated muscle. J Cell Biol. 1977 Nov;75(2 Pt 1):366–380. doi: 10.1083/jcb.75.2.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dupuis D. E., Guilford W. H., Wu J., Warshaw D. M. Actin filament mechanics in the laser trap. J Muscle Res Cell Motil. 1997 Feb;18(1):17–30. doi: 10.1023/a:1018672631256. [DOI] [PubMed] [Google Scholar]
  7. Eagles D. A., DeAndrea G. A., Riordan G. P. The T-axial membrane system in striated muscles of the horseshoe crab. Tissue Cell. 1982;14(3):531–540. doi: 10.1016/0040-8166(82)90045-3. [DOI] [PubMed] [Google Scholar]
  8. Erickson H. P. Stretching single protein molecules: titin is a weird spring. Science. 1997 May 16;276(5315):1090–1092. doi: 10.1126/science.276.5315.1090. [DOI] [PubMed] [Google Scholar]
  9. Fauver M. E., Dunaway D. L., Lilienfeld D. H., Craighead H. G., Pollack G. H. Microfabricated cantilevers for measurement of subcellular and molecular forces. IEEE Trans Biomed Eng. 1998 Jul;45(7):891–898. doi: 10.1109/10.686797. [DOI] [PubMed] [Google Scholar]
  10. Finer J. T., Mehta A. D., Spudich J. A. Characterization of single actin-myosin interactions. Biophys J. 1995 Apr;68(4 Suppl):291S–297S. [PMC free article] [PubMed] [Google Scholar]
  11. Ford L. E., Huxley A. F., Simmons R. M. The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol. 1981 Feb;311:219–249. doi: 10.1113/jphysiol.1981.sp013582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harrington W. F. A mechanochemical mechanism for muscle contraction. Proc Natl Acad Sci U S A. 1971 Mar;68(3):685–689. doi: 10.1073/pnas.68.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Huxley A. F. Muscular contraction. J Physiol. 1974 Nov;243(1):1–43. [PMC free article] [PubMed] [Google Scholar]
  14. Huxley A. F., Tideswell S. Filament compliance and tension transients in muscle. J Muscle Res Cell Motil. 1996 Aug;17(4):507–511. doi: 10.1007/BF00123366. [DOI] [PubMed] [Google Scholar]
  15. Huxley H. E., Stewart A., Sosa H., Irving T. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J. 1994 Dec;67(6):2411–2421. doi: 10.1016/S0006-3495(94)80728-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ishijima A., Doi T., Sakurada K., Yanagida T. Sub-piconewton force fluctuations of actomyosin in vitro. Nature. 1991 Jul 25;352(6333):301–306. doi: 10.1038/352301a0. [DOI] [PubMed] [Google Scholar]
  17. Kellermayer M. S., Smith S. B., Granzier H. L., Bustamante C. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science. 1997 May 16;276(5315):1112–1116. doi: 10.1126/science.276.5315.1112. [DOI] [PubMed] [Google Scholar]
  18. Kensler R. W., Levine R. J. An electron microscopic and optical diffraction analysis of the structure of Limulus telson muscle thick filaments. J Cell Biol. 1982 Feb;92(2):443–451. doi: 10.1083/jcb.92.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kishino A., Yanagida T. Force measurements by micromanipulation of a single actin filament by glass needles. Nature. 1988 Jul 7;334(6177):74–76. doi: 10.1038/334074a0. [DOI] [PubMed] [Google Scholar]
  20. Levine R. J., Kensler R. W. Structure of short thick filaments from Limulus muscle. J Mol Biol. 1985 Mar 20;182(2):347–352. doi: 10.1016/0022-2836(85)90351-1. [DOI] [PubMed] [Google Scholar]
  21. Levine R. J., Woodhead J. L., King H. A. The effect of calcium activation of skinned fiber bundles on the structure of Limulus thick filaments. J Cell Biol. 1991 May;113(3):573–583. doi: 10.1083/jcb.113.3.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Matsuno A., Kannda M., Okuda M. Ultrastructural studies on paramyosin core filaments from native thick filaments in catch muscles. Tissue Cell. 1996 Aug;28(4):501–505. doi: 10.1016/s0040-8166(96)80036-x. [DOI] [PubMed] [Google Scholar]
  23. Millman B. M., Elliott G. F. An x-ray diffraction study of contracting molluscan smooth muscle. Biophys J. 1972 Nov;12(11):1405–1414. doi: 10.1016/S0006-3495(72)86171-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nonomura Y. Fine structure of the thick filament in molluscan catch muscle. J Mol Biol. 1974 Sep 15;88(2):445–455. doi: 10.1016/0022-2836(74)90494-x. [DOI] [PubMed] [Google Scholar]
  25. Panté N. Paramyosin polarity in the thick filament of molluscan smooth muscles. J Struct Biol. 1994 Sep-Oct;113(2):148–163. doi: 10.1006/jsbi.1994.1047. [DOI] [PubMed] [Google Scholar]
  26. Pollack G. H. The cross-bridge theory. Physiol Rev. 1983 Jul;63(3):1049–1113. doi: 10.1152/physrev.1983.63.3.1049. [DOI] [PubMed] [Google Scholar]
  27. Saito K., Aoki T., Aoki T., Yanagida T. Movement of single myosin filaments and myosin step size on an actin filament suspended in solution by a laser trap. Biophys J. 1994 Mar;66(3 Pt 1):769–777. doi: 10.1016/s0006-3495(94)80853-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sellers J. R., Cuda G., Wang F., Homsher E. Myosin-specific adaptations of the motility assay. Methods Cell Biol. 1993;39:23–49. doi: 10.1016/s0091-679x(08)60159-4. [DOI] [PubMed] [Google Scholar]
  29. Siegman M. J., Mooers S. U., Li C., Narayan S., Trinkle-Mulcahy L., Watabe S., Hartshorne D. J., Butler T. M. Phosphorylation of a high molecular weight (approximately 600 kDa) protein regulates catch in invertebrate smooth muscle. J Muscle Res Cell Motil. 1997 Dec;18(6):655–670. doi: 10.1023/a:1018683823020. [DOI] [PubMed] [Google Scholar]
  30. Sobieszek A. The fine structure of the contractile apparatus of the anterior byssus retractor muscle of Mytilus edulis. J Ultrastruct Res. 1973 May;43(3):313–343. doi: 10.1016/s0022-5320(73)80041-3. [DOI] [PubMed] [Google Scholar]
  31. Szent-Györgyi A. G., Cohen C., Kendrick-Jones J. Paramyosin and the filaments of molluscan "catch" muscles. II. Native filaments: isolation and characterization. J Mol Biol. 1971 Mar 14;56(2):239–258. doi: 10.1016/0022-2836(71)90462-1. [DOI] [PubMed] [Google Scholar]
  32. Tajima Y., Makino K., Hanyuu T., Wakabayashi K., Amemiya Y. X-ray evidence for the elongation of thin and thick filaments during isometric contraction of a molluscan smooth muscle. J Muscle Res Cell Motil. 1994 Dec;15(6):659–671. doi: 10.1007/BF00121073. [DOI] [PubMed] [Google Scholar]
  33. Tskhovrebova L., Trinick J., Sleep J. A., Simmons R. M. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature. 1997 May 15;387(6630):308–312. doi: 10.1038/387308a0. [DOI] [PubMed] [Google Scholar]
  34. Twarog B. M. The regulation of catch in molluscan muscle. J Gen Physiol. 1967 Jul;50(6 Suppl):157–169. doi: 10.1085/jgp.50.6.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wakabayashi K., Sugimoto Y., Tanaka H., Ueno Y., Takezawa Y., Amemiya Y. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J. 1994 Dec;67(6):2422–2435. doi: 10.1016/S0006-3495(94)80729-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walcott B., Dewey M. M. Length-tension relation in Limulus striated muscle. J Cell Biol. 1980 Oct;87(1):204–208. doi: 10.1083/jcb.87.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES