Mechanosensitive channel properties and membrane mechanics in mouse dystrophic myotubes

Journal of Physiology

Volumn 581, Issue 1, 2007, Pages 369-387

  Suchyna, Thomas M ^a   Sachs, Frederick ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CALCIUM; CALCIUM ION; DYSTROPHIN; ION CHANNEL; CATION CHANNEL; ION TRANSPORT AFFECTING AGENT; MECHANOSENSITIVE CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM TRANSPORT; CAVEOLA; CELL MEMBRANE DEPOLARIZATION; CELL STIMULATION; CHANNEL GATING; CONTROLLED STUDY; CYTOSKELETON; ELECTROPHYSIOLOGY; LATENT PERIOD; MECHANICAL STRESS; MOUSE; MUSCLE FIBRIL; MUSCLE RELAXATION; MUSCULAR DYSTROPHY; NONHUMAN; PATCH CLAMP; PATHOPHYSIOLOGY; PRIORITY JOURNAL; STRAIN DIFFERENCE; TRANSPORT KINETICS; TRANSVERSE TUBULAR SYSTEM; VISCOSITY; WILD TYPE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE; ELECTRIC CAPACITANCE; MUSCLE FIBER MEMBRANE STEADY POTENTIAL; MYOTUBE; PATCH CLAMP TECHNIQUE;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CELL MEMBRANE; CELLS, CULTURED; CYTOSKELETON; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; ION CHANNELS; MECHANORECEPTORS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE FIBERS; MUSCULAR DYSTROPHIES; PATCH-CLAMP TECHNIQUES;

EID: 34248172959     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.125021     Document Type: Article

References (82)

1. Akinlaja J & Sachs F (1998). The breakdown of cell membranes by electrical and mechanical stress. Biophys J 75, 247-254.
2. Akitake B, Anishkin A & Sukharev S (2005). The 'dashpot'mechanism of stretch-dependent gating in MscS. J Gen Physiol 125, 143-154.
3. Alderton JM & Steinhardt RA (2000 a). Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J Biol Chem 275, 9452-9460.
4. Alderton JM & Steinhardt RA (2000 b). How calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. Trends Cardiovasc Med 10, 268-272.
5. Anderson RG (1998). The caveolae membrane system. Annu Rev Biochem 67, 199-225.
6. Bausch AR, Ziemann F, Boulbitch AA, Jacobson K & Sackmann E (1998). Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. Biophys J 75, 2038-2049.
7. Bett GCL & Sachs F (2000). Whole-cell mechanosensitive currents in rat ventricular myocytes activated by direct stimulation. J Membr Biol 173, 255-263.
8. Blake DJ, Weir A, Newey SE & Davies KE (2002). Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82, 291-329.
9. Bonilla E, Schmidt B, Samitt CE, Miranda AF, Hays AP, DeOlivera AB, Chang HW, Servidei S, Ricci E & Younger DS (1988). Normal and dystrophin-deficient muscle fibers in carriers of the gene for Duchenne muscular dystrophy. Am J Pathol 133, 440-445.
10. Bowman CL, Gottlieb PA, Suchyna TM, Murphy YK & Sachs F (2006). Mechanosensitive ion channels and the peptide inhibitor GsMTx-4: History, properties, mechanisms and pharmacology. Toxicon 49, 249-270.
11. 2+ influx channels by regulating plasma membrane localization of TRPC1. J Biol Chem 278, 27208-27215.
12. Campbell KP & Kahl SD (1989). Association of dystrophin and an integral membrane glycoprotein. Nature 338, 259-262.
13. 2+ homeostasis and of survival in collagenase-isolated muscle fibres from normal and mdx mice. J Physiol 542, 855-865.
14. De Deyne PG (2000). Formation of sarcomeres in developing myotubes: Role of mechanical stretch and contractile activation. Am J Physiol Cell Physiol 279, C1801-C1811.
15. Ducret T, Vandebrouck C, Cao ML, Lebacq J & Gailly P (2006). Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J Physiol 575, 913-924.
16. Dulhunty AF & Franzini-Armstrong C (1975). The relative contributions of the folds and caveolae to the surface membrane of frog skeletal muscle fibres at different sarcomere lengths. J Physiol 250, 513-539.
17. Evans E, Heinrich V, Ludwig F & Rawicz W (2003). Dynamic tension spectroscopy and strength of biomembranes. Biophys J 85, 2342-2350.
18. Franco A Jr & Lansman JB (1990). Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 344, 670-673.
19. Franco-Obregon A Jr & Lansman JB (1994). Mechanosensitive ion channels in skeletal muscle from normal and dystrophic mice. J Physiol 481, 299-309.
20. Franco-Obregon A & Lansman JB (2002). Changes in mechanosensitive channel gating following mechanical stimulation in skeletal muscle myotubes from the mdx mouse. J Physiol 539, 391-407.
21. Fung YC (1981). Biomechanics. Springer Verlag, New York.
22. Gailly P (2002). New aspects of calcium signaling in skeletal muscle cells: Implications in Duchenne muscular dystrophy. Biochim Biophys Acta 1600, 38-44.
23. Galbiati F, Engelman JA, Volonte D, Zhang XL, Minetti C, Li M, Hou H Jr, Kneitz B, Edelmann W & Lisanti MP (2001 a). Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and t-tubule abnormalities. J Biol Chem 276, 21425-21433.
24. Galbiati F, Razani B & Lisanti MP (2001 b). Caveolae and caveolin-3 in muscular dystrophy. Trends Mol Med 7, 435-441.
25. 2+ current and charge movement in adult single human skeletal muscle fibres. J Physiol 454, 183-196.
26. Gil Z, Silberberg SD & Magleby KL (1999). Voltage-induced membrane displacement in patch pipettes activates mechanosensitive channels. Proc Natl Acad Sci U S A 96, 14594-14599.
27. Grouselle M, Stuyvers B, Bonoron-Adele S, Besse P & Georgescauld D (1991). Digital-imaging microscopy analysis of calcium release from sarcoplasmic reticulum in single rat cardiac myocytes. Pflugers Arch 418, 109-119.
28. Guharay F & Sachs F (1984). Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol 352, 685-701.
29. Hamill OP & McBride DW Jr (1992). Rapid adaptation of single mechanosensitive channels in Xenopus oocytes. Proc Natl Acad Sci U S A 89, 7462-7466.
30. Honore E, Patel AJ, Chemin J, Suchyna T & Sachs F (2006). Desensitization of mechano-gated K2P channels. Proc Natl Acad Sci U S A 103, 6859-6864.
31. Imbert N, Vandebrouck C, Duport G, Raymond G, Hassoni AA, Constantin B, Cullen MJ & Cognard C (2001). Calcium currents and transients in co-cultured contracting normal and Duchenne muscular dystrophy human myotubes. J Physiol 534, 343-355.
32. 2+-permeable growth factor-regulated channel. J Cell Biol 161, 957-967.
33. Kelly AM (1971). Sarcoplasmic reticulum and T-tubules in differentiating rat skeletal muscle. J Cell Biol 49, 335-344.
34. Kelly SM & Price NC (1997). The application of circular dichroism to studies of protein folding and unfolding. Biochim Biophys Acta 1338, 161-185.
35. Kosawada T, Inoue K & Schmid-Schonbein GW (2005). Mechanics of curved plasma membrane vesicles: Resting shapes, membrane curvature, and in-plane shear elasticity. J Biomech Eng 127, 229-236.
36. Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA, Ochoa GC, Farsad K, De Wenk MR & CP (2002). Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297, 1193-1196.
37. Leijendekker WJ, Passaquin AC, Metzinger L & Ruegg UT (1996). Regulation of cytosolic calcium in skeletal muscle cells of the mdx mouse under conditions of stress. Br J Pharmacol 118, 611-616.
38. Li H, Cook JD, Terry M, Spitzer NC & Ferrari MB (2004). Calcium transients regulate patterned actin assembly during myofibrillogenesis. Dev Dyn 229, 231-242.
39. Li KX & Sperelakis N (1994). Electrogenic Na-K pump current in rat skeletal myoballs. J Cell Physiol 159, 181-186.
40. Lollike K, Borregaard N & Lindau M (1998). Capacitance flickers and pseudoflickers of small granules, measured in the cell-attached configuration. Biophys J 75, 53-59.
41. Lorenzon P, Giovannelli A, Ragozzino D, Eusebi F & Ruzzier F (1997). Spontaneous and repetitive calcium transients in C2C12 mouse myotubes during in vitro myogenesis. Eur J Neurosci 9, 800-808.
42. McCarter GC & Steinhardt RA (2000). Increased activity of calcium leak channels caused by proteolysis near sarcolemmal ruptures. J Membr Biol 176, 169-174.
43. Marchand E, Constantin B, Vandebrouck C, Raymond G & Cognard C (2001). Calcium homeostasis and cell death in Sol8 dystrophin-deficient cell line in culture. Cell Calcium 29, 85-96.
44. Markin VS & Sachs F (2004). Thermodynamics of mechanosensitivity: lipid shape, membrane deformation and anesthesia. Biophys J 86, 370A.
45. Maroto R, Raso A, Wood TG, Kurosky A, Martinac B & Hamill OP (2005). TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7, 179-185.
46. Morris CE (2001). Mechanoprotection of the plasma membrane in neurons and other non-erythroid cells by the spectrin-based membrane skeleton. Cell Mol Biol Lett 6, 703-720.
47. Morris CE & Horn R (1991). Failure to elicit neuronal macroscopic mechanosensitive currents anticipated by single-channel studies. Science 251, 1246-1249.
48. Morris CE & Sigurdson WJ (1989). Stretch-inactivated ion channels coexist with stretch-activated ion channels. Science 243, 807-809.
49. Mukhin SI & Baoukina SV (2004). Inter-layer slide and stress relaxation in a bilayer lipid membrane in the patch-clamp setting. Biol Membr 21, 506-517.
50. Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M & Imaizumi Y (2003). TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93, 829-838.
51. Nakamura TY, Iwata Y, Sampaolesi M, Hanada H, Saito N, Artman M, Coetzee WA & Shigekawa M (2001). Stretch-activated cation channels in skeletal muscle myotubes from sarcoglycan-deficient hamsters. Am J Physiol Cell Physiol 281, C690-C699.
52. Nishizaka T, Seo R, Tadakuma H, Kinosita K Jr & Ishiwata S (2000). Characterization of single actomyosin rigor bonds: Load dependence of lifetime and mechanical properties. Biophys J 79, 962-974.
53. + channels in adult rat atrial myocytes. Prog Biophys Mol Biol 82, 121-135.
54. Opsahl LR & Webb WW (1994). Lipid-glass adhesion in giga-sealed patch-clamped membranes. Biophys J 66, 75-79.
55. Parton RG, Way M, Zorzi N & Stang E (1997). Caveolin-3 associates with developing T-tubules during muscle differentiation. J Cell Biol 136, 137-154.
56. Pasternak C, Wong S & Elson EL (1995). Mechanical function of dystrophin in muscle cells. J Cell Biol 128, 355-361.
57. Petrof BJ, Shrager JB, Stedman HH, Kelly AM & Sweeney HL (1993). Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci U S A 90, 3710-3714.
58. Rybakova IN, Patel JR & Ervasti JM (2000). The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J Cell Biol 150, 1209-1214.
59. Saadat L, Pittman L & Menhart N (2006). Structural cooperativity in spectrin type repeats motifs of dystrophin. Biochim Biophys Acta 1764, 943-954.
60. Sachs F (1990). Stretch-sensitive ion channels. Neuroscience 2, 49-57.
61. Small DL & Morris CE (1994). Delayed activation of single mechanosensitive channels in Lymnaea neurons. Am J Physiol Cell Physiol 267, C598-C606.
62. Sokabe M & Sachs F (1990). The structure and dynamics of patch-clamped membranes: A study by differential interference microscopy. J Cell Biol 111, 599-606.
63. Sokabe M, Sachs F & Jing Z (1991). Quantitative video microscopy of patch clamped membranes -stress, strain, capacitance and stretch channel activation. Biophys J 59, 722-728.
64. Solsona C, Innocenti B & Fernandez JM (1998). Regulation of exocytotic fusion by cell inflation. Biophys J 74, 1061-1073.
65. Sombers LA, Hanchar HJ, Colliver TL, Wittenberg N, Cans A, Arbault S, Amatore C & Ewing AG (2004). The effects of vesicular volume on secretion through the fusion pore in exocytotic release from PC12 cells. J Neurosci 24, 303-309.
66. Sotgia F, Lee JK, Das K, Bedford M, Petrucci TC, Macioce P, Sargiacomo M, Bricarelli FD, Minetti C, Sudol M & Lisanti MP (2000). Caveolin-3 directly interacts with the C-terminal tail of beta -dystroglycan. Identification of a central WW-like domain within caveolin family members. J Biol Chem 275, 38048-38058.
67. Spassova MA, Hewavitharana T, Xu W, Soboloff J & Gill DL (2006). A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci U S A 103, 16586-16591.
68. Suchyna TM, Besch SR & Sachs F (2004 a). Dynamic regulation of mechanosensitive channels: Capacitance used to monitor patch tension in real time. Phys Biol 1, 1-18.
69. Suchyna TM, Johnson JH, Clemo HF, Huang ZH, Gage DA, Baumgarten CM & Sachs F (2000). Identification of a peptide toxin from Grammostola spatulata spider venom that blocks stretch activated channels. J Gen Physiol 115, 583-598.
70. Suchyna TM & Sachs F (2005). Membrane-cytoskeletal interface and mechanosensitive channels. In Cardiac Mechano-Electric Feedback and Arrhythmias, from Pipette to Patient, ed. Kohl P, Sachs F & Franz MR, pp. 42-52. Elsevier Saunders, Philadelphia.
71. Suchyna TM, Tape SE, Koeppe RE, Andersen OS, Sachs F & Gottlieb PA (2004 b). Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature 430, 235-240.
72. Sukharev S, Sigurdson W, Kung C & Sachs F (1999). Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J Gen Physiol 113, 525-539.
73. Takayama I, Fujii Y, Terada N, Baba T, Kato Y, Fujino MA & Ohno S (2000). Topographical difference of cytoskeletal organization in smooth muscle cells of rat duodenum revealed by quick-freezing and deep-etching method. Histol Histopathol 15, 1059-1066.
74. Tang Z, Scherer PE, Okamoto T, Song K, Chu C, Kohtz DS, Nishimoto I, Lodish HF & Lisanti MP (1996). Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J Biol Chem 271, 2255-2261.
75. Thomsen P, Roepstorff K, Stahlhut M & van Deurs B (2002). Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 13, 238-250.
76. Thorn H, Stenkula KG, Karlsson M, Ortegren U, Nystrom FH, Gustavsson J & Stralfors P (2003). Cell surface orifices of caveolae and localization of caveolin to the necks of caveolae in adipocytes. Mol Biol Cell 14, 3967-3976.
77. Vaghy PL, Fang J, Wu W & Vaghy LP (1998). Increased caveolin-3 levels in mdx mouse muscles. FEBS Lett 431, 125-127.
78. Vandebrouck C, Duport G, Raymond G & Cognard C (2002). Hypotonic medium increases calcium permeant channels activity in human normal and dystrophic myotubes. Neurosci Lett 323, 239-243.
79. Wiggins P & Phillips R (2005). Membrane-protein interactions in mechanosensitive channels. Biophys J 88, 880-902.
80. Yeung EW, Head SI & Allen DG (2003). Gadolinium reduces short-term stretch-induced muscle damage in isolated mdx mouse muscle fibres. J Physiol 552, 449-458.
81. 2+ ] i and muscle damage in the mdx mouse. J Physiol 562, 367-380.
82. Zhang Y & Hamill OP (2000). On the discrepancy between whole-cell and membrane patch mechanosensitivity in Xenopus oocytes. J Physiol 523, 101-115.