Synergy between Piezo1 and Piezo2 channels confers high-strain mechanosensitivity to articular cartilage

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 47, 2014, Pages E5114-E5122

  Lee, Whasil ^a   Leddy, Holly A ^a   Chen, Yong ^a   Lee, Suk Hee ^a   Zelenski, Nicole A ^a   McNulty, Amy L ^a   Wu, Jason ^a   Beicker, Kellie N ^b   Coles, Jeffrey ^c   Zauscher, Stefan ^c   Grandl, Jörg ^a   Sachs, Frederick ^d   Guilak, Farshid ^a,c   Liedtke, Wolfgang B ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c Duke University   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

Cartilage; Cartilage injury; Chondrocyte; Mechanotransduction; Piezo

Indexed keywords

ION CHANNEL; MESSENGER RNA; PIEZO1 CHANNEL; PIEZO2 CHANNEL; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; PIEZO1 PROTEIN, MOUSE; PIEZO2 PROTEIN, MOUSE;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; ATOMIC FORCE MICROSCOPY; BLADDER; CALCIUM SIGNALING; CARTILAGE CELL; CARTILAGE INJURY; CELL DEATH; CELL MEMBRANE; ELECTRIC CURRENT; ELECTROPHYSIOLOGY; EXPERIMENTAL PIG; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; LUNG; MALE; MECHANICAL STIMULATION; MECHANICAL STRESS; MECHANOTRANSDUCTION; NONHUMAN; OSTEOARTHRITIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TRIGEMINUS GANGLION; WHOLE CELL PATCH CLAMP; ANIMAL; GENETICS; MOUSE; PHYSIOLOGY;

ANIMALS; CALCIUM SIGNALING; CARTILAGE, ARTICULAR; CHONDROCYTES; ION CHANNELS; MICE; RNA, SMALL INTERFERING; STRESS, MECHANICAL;

EID: 84912572057     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1414298111     Document Type: Article

References (82)

1. Guilak F (2011) Biomechanical factors in osteoarthritis. Best Pract Res Clin Rheumatol 25(6):815-823.
2. Grodzinsky AJ, Levenston ME, Jin M, Frank EH (2000) Cartilage tissue remodeling in response to mechanical forces. Annu Rev Biomed Eng 2:691-713.
3. Fitzgerald JB, et al. (2004) Mechanical compression of cartilage explants induces multiple time-dependent gene expression patterns and involves intracellular calcium and cyclic AMP. J Biol Chem 279(19):19502-19511.
4. Quinn TM, Grodzinsky AJ, Buschmann MD, Kim YJ, Hunziker EB (1998) Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants. J Cell Sci 111(Pt 5):573-583.
5. Ragan PM, et al. (1999) Down-regulation of chondrocyte aggrecan and type-II collagen gene expression correlates with increases in static compression magnitude and duration. J Orthop Res 17(6):836-842.
6. Valhmu WB, et al. (1998) Load-controlled compression of articular cartilage induces a transient stimulation of aggrecan gene expression. Arch Biochem Biophys 353(1):29-36.
7. Guilak F, Sah R, Setton LA (1997) Physical regulation of cartilage metabolism. Basic Orthopaedic Biomechanics, eds Mow VC, Hayes WC (Lippincott-Raven, Philadelphia), pp 179-207.
8. Stevens AL, Wishnok JS, White FM, Grodzinsky AJ, Tannenbaum SR (2009) Mechanical injury and cytokines cause loss of cartilage integrity and upregulate proteins associated with catabolism, immunity, inflammation, and repair. Mol Cell Proteomics 8(7): 1475-1489.
9. Lawrence RC, et al.; National Arthritis Data Workgroup (2008) Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum 58(1):26-35.
10. Brown TD, Johnston RC, Saltzman CL, Marsh JL, Buckwalter JA (2006) Posttraumatic osteoarthritis: A first estimate of incidence, prevalence, and burden of disease. J Orthop Trauma 20(10):739-744.
11. Mobasheri A, et al. (2012) Potassium channels in articular chondrocytes. Channels (Austin) 6(6):416-425.
12. Wann AK, et al. (2012) Primary cilia mediate mechanotransduction through control of ATP-induced Ca2+ signaling in compressed chondrocytes. FASEB J 26(4):1663-1671.
13. Vincent TL, McLean CJ, Full LE, Peston D, Saklatvala J (2007) FGF-2 is bound to perlecan in the pericellular matrix of articular cartilage, where it acts as a chondrocyte mechanotransducer. Osteoarthritis Cartilage 15(7):752-763.
14. Chao PH, West AC, Hung CT (2006) Chondrocyte intracellular calcium, cytoskeletal organization, and gene expression responses to dynamic osmotic loading. Am J Physiol Cell Physiol 291(4):C718-C725.
15. Mobasheri A, Carter SD, Martín-Vasallo P, Shakibaei M (2002) Integrins and stretch activated ion channels; putative components of functional cell surface mechanoreceptors in articular chondrocytes. Cell Biol Int 26(1):1-18.
16. Kock LM, et al. (2009) RGD-dependent integrins are mechanotransducers in dynamically compressed tissue-engineered cartilage constructs. J Biomech 42(13):2177-2182.
17. Irianto J, et al. (2013) Osmotic challenge drives rapid and reversible chromatin condensation in chondrocytes. Biophys J 104(4):759-769.
18. Phan MN, et al. (2009) Functional characterization of TRPV4 as an osmotically sensitive ion channel in porcine articular chondrocytes. Arthritis Rheum 60(10):3028-3037.
19. Clark AL, Votta BJ, Kumar S, Liedtke W, Guilak F (2010) Chondroprotective role of the osmotically sensitive ion channel transient receptor potential vanilloid 4: Age- and sex-dependent progression of osteoarthritis in Trpv4-deficient mice. Arthritis Rheum 62(10):2973-2983.
20. O'Conor CJ, Leddy HA, Benefield HC, Liedtke WB, Guilak F (2014) TRPV4-mediated mechanotransduction regulates the metabolic response of chondrocytes to dynamic loading. Proc Natl Acad Sci USA 111(4):1316-1321.
21. Drexler S, Wann A, Vincent TL (2014) Are cellular mechanosensors potential therapeutic targets in osteoarthritis? Int J Clin Rheumatol 9(2):155-167.
22. Coste B, et al. (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330(6000):55-60.
23. Xiao R, Xu XZ (2010) Mechanosensitive channels: In touch with Piezo. Curr Biol 20(21): R936-R938.
24. Zarychanski R, et al. (2012) Mutations in the mechanotransduction protein PIEZO1 are associated with hereditary xerocytosis. Blood 120(9):1908-1915.
25. Miyamoto T, et al. (2012) Piezo1, a novel mechanosensor in the bladder urothelium. Neurourol Urodyn 31(6):1015-1017.
26. Gottlieb PA, Bae C, Gnanasambandam R, Nicolai C, Sachs F (2013) Piezo1 mutations identified in xerocytosis alter the inactivation rate. Biophys J 104(2):467A-467A.
27. Demolombe S, Duprat F, Honoré E, Patel A (2013) Slower Piezo1 inactivation in dehydrated hereditary stomatocytosis (xerocytosis). Biophys J 105(4):833-834.
28. Andolfo I, et al. (2013) Multiple clinical forms of dehydrated hereditary stomatocytosis arise from mutations in PIEZO1. Blood 121(19):3925-3935, S1-S12.
29. Eijkelkamp N, et al. (2013) A role for Piezo2 in EPAC1-dependent mechanical allodynia. Nat Commun 4:1682.
30. Woo SH, et al. (2014) Piezo2 is required for Merkel-cell mechanotransduction. Nature 509(7502):622-626.
31. Maksimovic S, et al. (2014) Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509(7502):617-621.
32. Gottlieb PA, Sachs F (2012) Piezo1: Properties of a cation selective mechanical channel. Channels (Austin) 6(4):214-219.
33. Guharay F, Sachs F (1984) Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. J Physiol 352:685-701.
34. Choi JB, et al. (2007) Zonal changes in the three-dimensional morphology of the chondron under compression: The relationship among cellular, pericellular, and extracellular deformation in articular cartilage. J Biomech 40(12):2596-2603.
35. Li Y, et al. (2013) Moderate dynamic compression inhibits pro-catabolic response of cartilage to mechanical injury, tumor necrosis factor-alpha and interleukin-6, but accentuates degradation above a strain threshold. Osteoarthritis Cartilage 21(12): 1933-1941.
36. Stolberg-Stolberg JA, et al. (2013) Effects of cartilage impact with and without fracture on chondrocyte viability and the release of inflammatory markers. J Orthop Res 31(8):1283-1292.
37. Wang N, Butler JP, Ingber DE (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260(5111):1124-1127.
38. Balasubramanian L, Ahmed A, Lo C-M, Sham JSK, Yip K-P (2007) Integrin-mediated mechanotransduction in renal vascular smooth muscle cells: Activation of calcium sparks. Am J Physiol Regul Integr Comp Physiol 293(4):R1586-R1594.
39. Krieg M, Dunn AR, Goodman MB (2014) Mechanical control of the sense of touch by β-spectrin. Nat Cell Biol 16(3):224-233.
40. Bae C, Gnanasambandam R, Nicolai C, Sachs F, Gottlieb PA (2013) Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1. Proc Natl Acad Sci USA 110(12):E1162-E1168.
41. Bae C, Sachs F, Gottlieb PA (2011) The mechanosensitive ion channel Piezo1 is inhibited by the peptide GsMTx4. Biochemistry 50(29):6295-6300.
42. Gottlieb PA, Suchyna TM, Sachs F (2007) Properties and mechanism of the mechanosensitive ion channel inhibitor GsMTx4, a therapeutic peptide derived from tarantula venom. Curr Top Membr 59:81-109.
43. Martinac B (2004) Mechanosensitive ion channels: Molecules of mechanotransduction. J Cell Sci 117(Pt 12):2449-2460.
44. Coste B (2012) [Piezo proteins form a new class of mechanically activated ion channels]. Med Sci (Paris) 28(12):1056-1057.
45. Vásquez V, Krieg M, Lockhead D, Goodman MB (2014) Phospholipids that contain polyunsaturated fatty acids enhance neuronal cell mechanics and touch sensation. Cell Reports 6(1):70-80.
46. Ferguson SM, De Camilli P (2012) Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 13(2):75-88.
47. Macia E, et al. (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10(6): 839-850.
48. Takamatsu A, et al. (2014) Verapamil protects against cartilage degradation in osteoarthritis by inhibiting Wnt/β-catenin signaling. PLoS ONE 9(3):e92699.
49. Sánchez JC, Danks TA, Wilkins RJ (2003) Mechanisms involved in the increase in intracellular calcium following hypotonic shock in bovine articular chondrocytes. Gen Physiol Biophys 22(4):487-500.
50. Suchyna TM, Sachs F (2007) Mechanosensitive channel properties and membrane mechanics in mouse dystrophic myotubes. J Physiol 581(Pt 1):369-387.
51. Yeung EW, et al. (2005) Effects of stretch-activated channel blockers on [Ca2+]i and muscle damage in the mdx mouse. J Physiol 562(Pt 2):367-380.
52. Erickson GR, Alexopoulos LG, Guilak F (2001) Hyper-osmotic stress induces volume change and calcium transients in chondrocytes by transmembrane, phospholipid, and G-protein pathways. J Biomech 34(12):1527-1535.
53. Ohashi T, Hagiwara M, Bader DL, Knight MM (2006) Intracellular mechanics and mechanotransduction associated with chondrocyte deformation during pipette aspiration. Biorheology 43(3-4):201-214.
54. D'Andrea P, Vittur F (1997) Propagation of intercellular Ca2+ waves in mechanically stimulated articular chondrocytes. FEBS Lett 400(1):58-64.
55. Barrett-Jolley R, Lewis R, Fallman R, Mobasheri A (2010) The emerging chondrocyte channelome. Front Physiol 1:135.
56. Sánchez JC, Powell T, Staines HM, Wilkins RJ (2006) Electrophysiological demonstration of voltage-activated H+ channels in bovine articular chondrocytes. Cell Physiol Biochem 18(1-3):85-90.
57. Martins RP, Finan JD, Guilak F, Lee DA (2012) Mechanical regulation of nuclear structure and function. Annu Rev Biomed Eng 14:431-455.
58. Perera PM, et al. (2010) Mechanical signals control SOX-9, VEGF, and c-Myc expression and cell proliferation during inflammation via integrin-linked kinase, B-Raf, and ERK1/2-dependent signaling in articular chondrocytes. Arthritis Res Ther 12(3):R106.
59. Spiteri C, Raizman I, Pilliar RM, Kandel RA (2010) Matrix accumulation by articular chondrocytes during mechanical stimulation is influenced by integrin-mediated cell spreading. J Biomed Mater Res A 94(1):122-129.
60. Mathieu PS, Loboa EG (2012) Cytoskeletal and focal adhesion influences on mesenchymal stem cell shape, mechanical properties, and differentiation down osteogenic, adipogenic, and chondrogenic pathways. Tissue Eng Part B Rev 18(6):436-444.
61. Vincent TL (2013) Targeting mechanotransduction pathways in osteoarthritis: A focus on the pericellular matrix. Curr Opin Pharmacol 13(3):449-454.
62. Amin AK, Huntley JS, Bush PG, Simpson AH, Hall AC (2009) Chondrocyte death in mechanically injured articular cartilage-the influence of extracellular calcium. J Orthop Res 27(6):778-784.
63. Hu W, et al. (2012) Blockade of acid-sensing ion channels protects articular chondrocytes from acid-induced apoptotic injury. Inflammation Res 61(4):327-335.
64. Huser CA, Davies ME (2007) Calcium signaling leads to mitochondrial depolarization in impact-induced chondrocyte death in equine articular cartilage explants. Arthritis Rheum 56(7):2322-2334.
65. Rong C, et al. (2012) Inhibition of acid-sensing ion channels by amiloride protects rat articular chondrocytes from acid-induced apoptosis via a mitochondrial-mediated pathway. Cell Biol Int 36(7):635-641.
66. Liu YW, et al. (2011) Differential curvature sensing and generating activities of dynamin isoforms provide opportunities for tissue-specific regulation. Proc Natl Acad Sci USA 108(26):E234-E242.
67. Roux A, et al. (2010) Membrane curvature controls dynamin polymerization. Proc Natl Acad Sci USA 107(9):4141-4146.
68. Wiejak J, Wyroba E (2002) Dynamin: Characteristics, mechanism of action and function. Cell Mol Biol Lett 7(4):1073-1080.
69. Sauter E, Buckwalter JA, McKinley TO, Martin JA (2012) Cytoskeletal dissolution blocks oxidant release and cell death in injured cartilage. J Orthop Res 30(4):593-598.
70. Phillips DM, Haut RC (2004) The use of a non-ionic surfactant (P188) to save chondrocytes from necrosis following impact loading of chondral explants. J Orthop Res 22(5):1135-1142.
71. Kockskämper J, et al. (2008) The slow force response to stretch in atrial and ventricular myocardium from human heart: Functional relevance and subcellular mechanisms. Prog Biophys Mol Biol 97(2-3):250-267.
72. Bode F, Sachs F, Franz MR (2001) Tarantula peptide inhibits atrial fibrillation. Nature 409(6816):35-36.
73. Leddy HA, et al. (2014) Follistatin in chondrocytes: The link between TRPV4 channelopathies and skeletal malformations. FASEB J 28(6):2525-2537.
74. Liedtke W, et al. (2000) Vanilloid receptor-related osmotically activated channel (VROAC), a candidate vertebrate osmoreceptor. Cell 103(3):525-535.
75. Chen Y, et al. (2013) Temporomandibular joint pain: A critical role for Trpv4 in the trigeminal ganglion. Pain 154(8):1295-1304.
76. Guilak F, Erickson GR, Ting-Beall HP (2002) The effects of osmotic stress on the viscoelastic and physical properties of articular chondrocytes. Biophys J 82(2):720-727.
77. Li J, et al. (2011) TRPV4-mediated calcium influx into human bronchial epithelia upon exposure to diesel exhaust particles. Environ Health Perspect 119(6):784-793.
78. Yeo M, Berglund K, Augustine G, Liedtke W (2009) Novel repression of Kcc2 transcription by REST-RE-1 controls developmental switch in neuronal chloride. J Neurosci 29(46):14652-14662.
79. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101-1108.
80. Coste B, et al. (2012) Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483(7388):176-181.
81. Suchyna TM, et al. (2004) Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature 430(6996):235-240.
82. Amin AK, et al. (2011) Hyperosmolarity protects chondrocytes from mechanical injury in human articular cartilage: An experimental report. J Bone Joint Surg Br 93(2): 277-284.