Cell volume regulation in chondrocytes

Cellular Physiology and Biochemistry

Volumn 28, Issue 6, 2011, Pages 1111-1122

  Lewis, Rebecca ^a   Feetham, Claire H ^a   Barrett Jolley, Richard ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Cell Volume Regulation; Ion channel; Membrane potential; Potassium ion channel; RVD; RVI; TRPV4; TRPV5; TRPV6

Indexed keywords

CHLORIDE ION; COTRANSPORTER; POTASSIUM ION; SODIUM ION; VANILLOID RECEPTOR 4; VANILLOID RECEPTOR 5;

APOPTOSIS; ARTHRALGIA; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL DAMAGE; CELL FUNCTION; CELL SWELLING; CELL VOLUME; ENCHONDRAL OSSIFICATION; EXTRACELLULAR MATRIX; HUMAN; HYPERTROPHY; NONHUMAN; OSMOLARITY; OSTEOARTHRITIS; PRIORITY JOURNAL; REVIEW; WATER CONTENT;

EID: 83755182899     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000335847     Document Type: Review

References (149)

1. Stockwell RA: Chondrocytes. J Clin Patholog1978;31:7-13.
2. Urban JP: The chondrocyte: A cell under pressure. Br J Rheumatol 1994;33:901-908. (Pubitemid 24324803)
3. Broom ND, Marra DL: New structural concepts of articular-cartilage demonstrated with a physical model. Connect Tissue Res 1985;14:1-8.
4. Buckwalter JA, Mower D, Ungar R, Schaeffer J, Ginsberg B: Morphometric analysis of chondrocyte hypertrophy. J Bone Joint Surg Am 1986;68A:243-255. (Pubitemid 16108702)
5. Cowell HR, Hunziker EB, Rosenberg L: The role of hypertrophic chondrocytes in endochondral ossification and in the development of secondary centers of ossification. J Bone Joint Surg Am 1987;69A:159-161.
6. Hunziker EB, Schenk RK: Physiological mechanisms adopted by chondrocytes in regulating longitudinal bone growth in rats. J Physiol 1989;414:55-71. (Pubitemid 19177291)
7. Breur GJ, Vanenkevort BA, Farnum CE, Wilsman NJ: Linear relationship between the volume of hypertrophic chondrocytes and the rate of longitudinal bone-growth in growth plates. J Orthop Res 1991;9:348-359.
8. Bush PG, Hall AC, Macnicol MF: New insights into function of the growth plate clinical observations, chondrocyte enlargement and a possible role for membrane transporters. J Bone Joint Surg Br 2008;90:1541-1547.
9. Adolphe M, Ronot X, Jaffray P, Hecquet C, Fontagne J, Lechat P: Effects of donor's age on growth kinetics of rabbit articular chondrocytes in culture. Mech Ageing Dev 1983;23:191-198. (Pubitemid 14181213)
10. Paukkonen K, Selkainaho K, Jurvelin J, Kiviranta I, Helminen HJ: Cells and nuclei of articular-cartilage chondrocytes in young-rabbits enlarged after nonstrenuous physical exercise. J Anat 1985;142:13-20. (Pubitemid 16244284)
11. Lang F, Ritter M, Gamper N, Huber S, Fillon S, Tanneur V, Lepple-Wienhues A, Szabo I, Gulbins E: Cell volume in the regulation of cell proliferation and apoptotic cell death. Cell Physiol Biochem 2000;10:417-428. (Pubitemid 32008925)
12. Borrelli J, Tinsley K, Ricci WM, Burns M, Karl IE, Hotchkiss R: Induction of chondrocyte apoptosis following impact load. J Orthop Trauma 2003;17:635-641. (Pubitemid 37428289)
13. Guilak F: Compression-induced changes in the shape and volume of the chondrocyte nucleus. J Biomech 1995;28:1529-1541. (Pubitemid 26004298)
14. Guilak F, Ratcliffe A, Mow VC: Chondrocyte deformation and local tissue strain in articular cartilage: A confocal microscopy study. J Orthop Res 1995;13:410-421.
15. Buschmann MD, Hunziker EB, Kim YJ, Grodzinsky AJ: Altered aggrecan synthesis correlates with cell and nucleus structure in statically compressed cartilage. J Cell Sci 1996;109:499-508. (Pubitemid 26057130)
16. Wu JZ, Herzog W, Epstein M: Modelling of location-and time-dependent deformation of chondrocytes during cartilage loading. J Biomech 1999;32:563-572. (Pubitemid 29219703)
17. Clark AL, Barclay LD, Matyas JR, Herzog W: In situ chondrocyte deformation with physiological compression of the feline patellofemoral joint. J Biomech 2003;36:553-568. (Pubitemid 36207586)
18. Freeman PM, Natarajan RN, Kimura JH, Andriacchi TP: Chondrocyte cells respond mechanically to compressive loads. J Orthop Res 1994;12:311-320. (Pubitemid 24181134)
19. Jones WR, Ting-Beall HP, Lee GM, Kelley SS, Hochmuth RM, Guilak F: Alterations in the young's modulus and volumetric properties of chondrocytes isolated from normal and osteoarthritic human cartilage. J Biomech 1999;32:119-127. (Pubitemid 29062274)
20. Maeda S, Nishida J, Sato T, Inomata Y, Shimamura T, Horiuchi S: Changes in microstructure and gene expression of articular chondrocytes cultured in a tube under mechanical stress. Osteoarthritis Cartilage 2005;13:154-161. (Pubitemid 40220806)
21. Wu QQ, Chen Q: Mechanoregulation of chondrocyte proliferation, maturation, and hypertrophy: Ion-channel dependent transduction of matrix deformation signals. Exp Cell Res 2000;256:383-391. (Pubitemid 30244197)
22. Chou MC, Tsai PH, Huang GS, Lee HS, Lee CH, Lin MH, Lin CY, Chung HW: Correlation between the mr t2 value at 4.7 t and relative water content in articular cartilage in experimental osteoarthritis induced by acl transection. Osteoarthr Cartilage 2009;17:441-447.
23. Venn M, Maroudas A: Chemical composition and swelling of normal and osteoarthrotic femoral-head cartilage .1. Chemical composition. Ann Rheum Dis 1977;36:121-129. (Pubitemid 8078656)
24. Mankin HJ, Thrasher AZ: Water-content and binding in normal and osteoarthritic human cartilage. J Bone Joint Surg 1975;57:76-80.
25. Mosher TJ, Liu Y, Torok CM: Functional cartilage mri t2 mapping: Evaluating the effect of age and training on knee cartilage response to running. Osteoarthritis Cartilage 2010;18:358-364.
26. Erickson GR, Alexopoulos LG, Guilak F: Hyper-osmotic stress induces volume change and calcium transients in chondrocytes by transmembrane, phospholipid, and g-protein pathways. J Biomech 2001;34:1527-1535. (Pubitemid 33041369)
27. Pritchard S, Erickson GR, Guilak F: Hyperosmotically induced volume change and calcium signaling in intervertebral disk cells: The role of the actin cytoskeleton. Biophys J 2002;83:2502-2510. (Pubitemid 35265744)
28. Bush PG, Hall AC: Regulatory volume decrease (rvd) by isolated and in situ bovine articular chondrocytes. J Cell Physiol 2001;187:304-314. (Pubitemid 32378355)
29. Bush PG, Hall AC: The osmotic sensitivity of isolated and in situ bovine articular chondrocytes. J Orthop Res 2001;19:768-778. (Pubitemid 32799061)
30. Kerrigan MJP, Hall AC: Control of chondrocyte regulatory volume decrease (rvd) by [Ca2+]i and cell shape. Osteoarthritis Cartilage 2008;16:312-322. (Pubitemid 351309184)
31. Lang F, Busch GL, Ritter M, Välkl H, Waldegger S, Gulbins E, Häussinger D: Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998;78:247-306. (Pubitemid 28070981)
32. Hoffmann EK, Lambert IH, Pedersen SF: Physiology of cell volume regulation in vertebrates. Physiol Rev 2009;89:193-277.
33. Errington RJ, Hall AC: Volume regulatory properties of porcine articular chondrocytes measured in cartilage explants using confocal microscopy. J Physiol 1995;482:P12-P13.
34. Starks I, Hall AC: Activation of K+ transport pathways of isolated bovine articular chondrocytes following osmotic perturbation. J Physiol 1995;482:P18-19.
35. Hall AC, Bush PG: The role of a swellingactivated taurine transport pathway in the regulation of articular chondrocyte volume. Europ J Physiol Pflugers Arch 2001;442:771-781. (Pubitemid 32783687)
36. Kerrigan MJP, Hook CSV, Qusous A, Hall AC: Regulatory volume increase (rvi) by in situ and isolated bovine articular chondrocytes. J Cell Physiol 2006;209:481-492. (Pubitemid 44484639)
37. Liang HT, Feng XC, Ma TH: Water channel activity of plasma membrane affects chondrocyte migration and adhesion. Clin Exp Pharmacol Physiol 2008;35:7-10.
38. Mobasheri A, Marples D: Expression of the aqp-1 water channel in normal human tissues: A semiquantitative study using tissue microarray technology. Am J Physiol Cell Physiol 2004;286:C529-537. (Pubitemid 38292658)
39. Mobasheri A, Trujillo E, Bell S, Carter SD, Clegg PD, Martin-Vasallo P, Marples D: Aquaporin water channels aqp1 and aqp3, are expressed in equine articular chondrocytes. Vet J 2004;168:143-150. (Pubitemid 39117917)
40. May H, Mobasheri A, Womack MD, Barrett-Jolley R: Functional expression of aquaporins in canine chondrocytes. Biophys J 2007;92:S543.
41. Hall AC: Volume-sensitive taurine transport in bovine articular chondrocytes. J Physiol 1995;484:755-766.
42. Sachs F: Mechanical transduction by membrane ion channels: A mini review. Mol Cell Biochem 1991;104:57-60.
43. Shakibaei M, Mobasheri A: Beta1-integrins co-localize with na, k-atpase, epithelial sodium channels (enac) and voltage activated calcium channels (vacc) in mechanoreceptor complexes of mouse limb-bud chondrocytes. Histol Histopathol 2003;18:343-351. (Pubitemid 36362050)
44. Mobasheri A, Carter SD, Martin-Vasallo P, Shakibaei M: Integrins and stretch activated ion channels; putative components of functional cell surface mechanoreceptors in articular chondrocytes. Cell Biol Int 2002;26:1-18. (Pubitemid 34174402)
45. Mouw JK, Imler SM, Levenston ME: Ionchannel regulation of chondrocyte matrix synthesis in 3d culture under static and dynamic compression. Biomech Modeling Mechanobiol 2006;6:33-41.
46. Voets T, Talavera K, Owsianik G, Nilius B: Sensing with trp channels. Nat Chem Biol 2005;1:85-92.
47. Guilak F, Leddy HA, Liedtke W: Transient receptor potential vanilloid 4 the sixth sense of the musculoskeletal system; in Zaidi M (ed): Skeletal biology and medicine. Wiley&Sons, New York 2010, vol 1192, pp 404-409.
48. Phan MN, Leddy HA, Votta BJ, Kumar S, Levy DS, Lipshutz DB, Lee SH, Liedtke W, Guilak F: Functional characterization of trpv4 as an osmotically sensitive ion channel in porcine articular chondrocytes. Arthritis Rheum 2009;60:3028-3037.
49. Clark AL, Votta BJ, Kumar S, Liedtke W, Guilak F: Chondroprotective role of the osmotically-sensitive ion channel trpv4: Age-and sex-dependent progression of osteoarthritis in trpv4 deficient mice. Arthritis Rheum 2010;62:2973-2983.
50. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T: Trpv4 calcium entry channel: A paradigm for gating diversity. Am J Physiol 2004;286:C195-C205. (Pubitemid 38146342)
51. Wilkins RJ, Fairfax TPA, Davies ME, Muzyamba MC, Gibson JS: Homeostasis of intracellular Ca2+ in equine chondrocytes: Response to hypotonic shock. Equine Vet J 2003;35:439-443. (Pubitemid 38698704)
52. Yellowley CE, Hancox JC, Donahue HJ: Effects of cell swelling on intracellular calcium and membrane currents in bovine articular chondrocytes. J Cell Biochem 2002;86:290-301. (Pubitemid 34743385)
53. Sanchez JC, Danks TA, Wilkins RJ: Mechanisms involved in the increase in intracellular calcium following hypotonic shock in bovine articular chondrocytes. Gen Physiol Biophys 2003;22:487-500. (Pubitemid 38324667)
54. Grandolfo M, Calabrese A, D'Andrea P: Mechanism of mechanically induced intercellular calcium waves in rabbit articular chondrocytes and in hig-82 synovial cells. J Bone Miner Res 1998;13:443-453. (Pubitemid 28146227)
55. Hall AC, Starks I, Shoults CL, Rashidbigi S: Pathways for K+ transport across the bovine articular chondrocyte membrane and their sensitivity to cell volume. Am J Physiol 1996;270:C1300-C1310.
56. Jensen B, Hertz M, Christophersen P, Madsen L: The Ca2+-activated K+ channel of intermediate conductance:A possible target for immune suppression. Expert Opin Ther Targets 2002;6:623-636. (Pubitemid 36054575)
57. Kobayashi T, Ikeda K, Kumanishi T: Inhibition by various antipsychotic drugs of the g-protein-activated inwardly rectifying K+ (girk) channels expressed in Xenopus oocytes. Brit J Pharmacol 2000;129:1716-1722. (Pubitemid 30219015)
58. Clark RB, Hatano N, Kondo C, Belke DD, Brown BS, Kumar S, Votta BJ, Giles WR: Voltage-gated K+ currents in mouse articular chondrocytes regulate membrane potential. Channels 2010;4:179-191.
59. Clark RB, Kondo C, Belke DD, Giles WR: Two-pore domain K+ channels regulate membrane potential of isolated human articular chondrocytes. J Physiol 2011;589:5071-5089.
60. Grandolfo M, Dandrea P, Martina M, Ruzzier F, Vittur F: Calcium-activated potassium channels in chondrocytes. Biochem Biophys Res Commun 1992;182:1429-1434.
61. Grandolfo M, Martina M, Ruzzier F, Vittur F: A potassium channel in cultured chondrocytes. Calcif Tissue Int 1990;47:302-307. (Pubitemid 20357376)
62. Martina M, Mozrzymas JW, Vittur F: Membrane stretch activates a potassium channel in pig articular chondrocytes. Biochim Biophys Acta 1997;1329:205-210. (Pubitemid 27466809)
63. Mobasheri A, Gent TC, Nash AI, Womack MD, Moskaluk CA, Barrett-Jolley R: Evidence for functional atp-sensitive (k(atp)) potassium channels in human and equine articular chondrocytes. Osteoarthritis Cartilage 2007;15:1-8. (Pubitemid 46117919)
64. Mobasheri A, Gent TC, Womack MD, Carter SD, Clegg PD, Barrett-Jolley R: Quantitative analysis of voltage-gated potassium currents from primary equine (equus caballus) and elephant (loxodonta africana) articular chondrocytes. Am J Physiol 2005;289:R172-R180. (Pubitemid 40874973)
65. Mobasheri A, Lewis R, Maxwell JEJ, Hill C, Womack M, Barrett-Jolley R: Characterization of a stretch-activated potassium channel in chondrocytes. J Cell Physiol 2010;223:511-518.
66. Mozrzymas JW, Martina M, Ruzzier F: A large-conductance voltage-dependent potassium channel in cultured pig articular chondrocytes. Europ J Physiol Pflugers Arch 1997;433:413-427. (Pubitemid 27065328)
67. Ponce A: Expression of voltage dependent potassium currents in freshly dissociated rat articular chondrocytes. Cell Physiol Biochem 2006;18:35-46.
68. Wilson JR, Duncan NA, Giles WR, Clark RB: A voltage-dependent K+ current contributes to membrane potential of acutely isolated canine articular chondrocytes. J Physiol 2004;557:93-104. (Pubitemid 38771639)
69. Wright M, Jobanputra P, Bavington C, Salter DM, Nuki G: Effects of intermittent pressure-induced strain on the electrophysiology of cultured human chondrocytes: Evidence for the presence of stretch-activated membrane ion channels. Clin Sci 1996;90:61-71. (Pubitemid 26010412)
70. Li P-C, Liang J-T, Huang H-T, Lin P-H, Wu S-N: Enhanced activity of Ca2+-activated K+ channels by 1-[2-hydroxy-3-p r o p y l-4-[ ( 1 h-t e t r a z o l-5-yl)butoxyl]phenyl] ethanone (ly-171883) in neuroendocrine and neuroblastoma cell lines. J Cell Physiol 2002;192:188-199. (Pubitemid 34747787)
71. Weiss H, Lang F: Ion channels activated by swelling of madin darby canine kidney (mdck) cells. J Mem Biol 1992;126:109-114.
72. Okumura N, Imai S, Toyoda F, Isoya E, Kumagai K, Matsuura H, Matsusue Y: Regulatory role of tyrosine phosphorylation in the swellingactivated chloride current in isolated rabbit articular chondrocytes. J Physiol 2009;587:3761-3776.
73. Isoya E, Toyoda F, Imai S, Okumura N, Kumagai K, Omatsu-Kanbe M, Kubo M, Matsuura H, Matsusue Y: Swellingactivated Cl-current in isolated rabbit articular chondrocytes: Inhibition by arachidonic acid. J Pharmacol Sci 2009;109:293-304.
74. Sugimoto T, Yoshino M, Nagao M, Ishii S, Yabu H: Voltage-gated ionic channels in cultured rabbit articular chondrocytes. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1996;115:223-232. (Pubitemid 27013436)
75. Tsuga K, Tohse N, Yoshino M, Sugimoto T, Yamashita T, Ishii S, Yabu H: Chloride conductance determining membrane potential of rabbit articular chondrocytes. J Mem Biol 2002;185:75-81. (Pubitemid 34075006)
76. Kunzelmann K, Tian Y, Martins J, Faria D, Kongsuphol P, Ousingsawat J, Thevenod F, Roussa E, Rock J, Schreiber R: Anoctamins. Europ J Physiol Pflügers Arch 2011;462:195-208.
77. Lewis R, Asplin K, Bruce G, Dart C, Mobasheri A, Barrett-Jolley R: The role of the membrane potential in chondrocyte volume regulation. J Cell Physiol 2011;226:2979-2986.
78. Wright MO, Stockwell RA, Nuki G: Response of plasma membrane to applied hydrostatic pressure in chondrocytes and fibroblasts. Connect Tissue Res 1992;28:49-70.
79. Funabashi K, Ohya S, Yamamura H, Hatano N, Muraki K, Giles W, Imaizumi Y: Accelerated Ca2+ entry by membrane hyperpolarization due to Ca2+-activated K+ channel activation in response to histamine in chondrocytes. Am J Physiol 2010;298:C786-C797.
80. Wilson JR, Clark RB, Banderali U, Giles WR: Measurement of the membrane potential in small cells using patch clamp methods. Channels 2011;5:455-454.
81. Friis UG, Praetorius HA, Knudsen T, Johansen T: Role of the Na+/K+-atpase in regulating the membrane potential in rat peritoneal mast cells. Brit J Pharmacol 1997;122:599-604. (Pubitemid 27453082)
82. Poignard C, Silve A, Campion F, Mir LM, Saut O, Schwartz L: Ion fluxes, transmembrane potential, and osmotic stabilization: A new dynamic electrophysiological model for eukaryotic cells. Eur Biophys J 2011;40:235-246.
83. Yurinskaya VE, Rubashkin AA, Vereninov AA: Balance of unidirectional monovalent ion fluxes in cells undergoing apoptosis: Why does Na+/K+ pump suppression not cause cell swelling J Physiol 2011;589:2197-2211.
84. Bush PG, Pritchard M, Loqman MY, Damron TA, Hall AC: A key role for membrane transporter nkcc1 in mediating chondrocyte volume increase in the mammalian growth plate. J Bone Miner Res 2010;25:1594-1603.
85. Ong SB, Shah D, Ousous A, Jarvis SM, Kerrigan MJP: Stimulation of regulatory volume increase (rvi) in avian articular chondrocytes by gadolinium chloride. Biochem Cell Biol 2010;88:505-512.
86. Qusous A, Geewan CSV, Greenwell P, Kerrigan MJP: Sirna-mediated inhibition of Na+-K+-2Cl-cotransporter (nkcc1) and regulatory volume increase in the chondrocyte cell line c-20/a4. J Mem Biol 2011;243:25-34.
87. Russell JM: Sodium-potassium-chloride cotransport. Physiol Rev 2000;80:211-276. (Pubitemid 30060565)
88. Lytle C: Activation of the avian erythrocyte Na-K-Cl cotransport protein by cell shrinkage, camp, fluoride, and calyculin-a involves phosphorylation at common sites. J Biol Chem 1997;272:15069-15077. (Pubitemid 27255519)
89. Sanchez JC, Wilkins RJ: Changes in intracellular calcium concentration in response to hypertonicity in bovine articular chondrocytes. Comp Biochem Physiol A Mol Integr Physiol 2004;137:173-182. (Pubitemid 38077009)
90. Hall AC, Horwitz ER, Wilkins RJ: The cellular physiology of articular cartilage. Exp Physiol 1996;81:535-545. (Pubitemid 26163088)
91. Mobasheri A, Hall AC, Urban JPG, France SJ, Smith AL: Immunologic and autoradiographic localisation of the Na+, K+-atpase in articular cartilage: Upregulation in response to changes in extracellular Na+ concentration. Int J Biochem Cell B 1997;29:649-657. (Pubitemid 27243993)
92. Hughes ALH, Pakhomova A, Brown PD: Regulatory volume increase in epithelial cells isolated from the mouse fourth ventricle choroid plexus involves Na+-H+ exchange but not Na+-K+-2Clcotransport. Brain Research 2010;1323:1-10.
93. Errington RJ, Fricker MD, Wood JL, Hall AC, White NS: Four-dimensional imaging of living chondrocytes in cartilage using confocal microscopy: A pragmatic approach. Am J Physiol 1997;272:C1040-C1051.
94. Deshayes CMP, Hall AC, Urban JPG: Effect of extracellular osmolality on porcine articular chondrocyte volume. J Physiol 1993;467:P214-214.
95. Benya PD, Shaffer JD: Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 1982;30:215-224. (Pubitemid 13237099)
96. Wehner F, Bondarava M, ter Veld F, Endl E, Nurnberger HR, Li T: Hypertonicityinduced cation channels. Acta Physiol 2006;187:21-25.
97. Migliati E, Meurice N, DuBois P, Fang JS, Somasekharan S, Beckett E, Flynn G, Yool AJ: Inhibition of aquaporin-1 and aquaporin-4 water permeability by a derivative of the loop diuretic bumetanide acting at an internal pore-occluding binding site. Mol Pharmacol 2009;76:105-112.
98. Bush PG, Pritchard M, Loqman MY, Damron TA, Hall AC: A key role for membrane transporter nkcc1 in mediating chondrocyte volume increase in the mammalian growth plate. J Bone Miner Res 2010;25:1594-1603.
99. Erickson GR, Northrup DL, Guilak F: Hypo-osmotic stress induces calciumdependent actin reorganization in articular chondrocytes. Osteoarthritis Cartilage 2003;11:187-197. (Pubitemid 36336424)
100. Dascalu A, Korenstein R, Oron Y, Nevo Z: A hyperosmotic stimulus regulates intracellular ph, calcium, and s-100 protein levels in avian chondrocytes. Biochem Biophys Res Commun 1996;227:368-373. (Pubitemid 26362811)
101. Kraft R: The Na+/Ca2+ exchange inhibitor kb-r7943 potently blocks trpc channels. Biochem Biophys Res Commun 2007;361:230-236. (Pubitemid 47102290)
102. Iwamoto T, Watano T, Shigekawa M: A novel isothiourea derivative selectively inhibits the reverse mode of Na+/Ca2+ exchange in cells expressing ncx1. J Biol Chem 1996;271:22391-22397. (Pubitemid 26304672)
103. Simpkin VL, Murray DH, Hall AP, Hall AC: Bicarbonate-dependent ph(i) regulation by chondrocytes within the superficial zone of bovine articular cartilage. J Cell Physiol 2007;212:600-609. (Pubitemid 47267530)
104. Mobasheri A, Errington RJ, Golding S, Hall AC, Urban JPG: Characterization of the Na+,K+-atpase in isolated bovine articular chondrocytes; molecular evidence for multiple alpha and beta isoforms. Cell Biology Int 1997;21:201-212. (Pubitemid 27283026)
105. Tattersall AL, Meredith D, Furla P, Shen MR, Ellory JC, Wilkins RJ: Molecular and functional identification of the Na+/H+ exchange isoforms nhe1 and nhe3 in isolated bovine articular chondrocytes. Cell Physiol Biochem 2003;13:215-222. (Pubitemid 36921040)
106. Wilkins RJ, Mobasheri A, Hall AC: Characterisation of Na+xH+ exchange in isolated bovine articular chondrocytes. FASEB J 1996;10:3843-3843.
107. Trujillo E, Alvarez de la Rosa D, Mobasheri A, Gonzalez T, Canessa CM, Martin-Vasallo P: Sodium transport systems in human chondrocytes. II. Expression of enac, Na+/K+/2Clcotransporter and Na+/H+ exchangers in healthy and arthritic chondrocytes. Histol Histopathol 1999;14:1023-1031. (Pubitemid 29447443)
108. Yamazaki N, Browning JA, Wilkins RJ: Modulation of Na+ x H+ exchange by osmotic shock in isolated bovine articular chondrocytes. Acta Physiol Scand 2000;169:221-228. (Pubitemid 30496934)
109. Barrett-Jolley R, Lewis R, Fallman R, Mobasheri A: The emerging chondrocyte channelome. Front Physiol 2010;1:135
110. Bondarava M, Li T, Endl E, Wehner F: Alpha-enac is a functional element of the hypertonicity-induced cation channel in hepg2 cells and it mediates proliferation. Pflugers Arch 2009;458:675-687.
111. Goldring MB, Goldring SR: Osteoarthritis. J Cell Physiol 2007;213:626-634. (Pubitemid 350058254)
112. Dieppe PA, Lohmander LS: Pathogenesis and management of pain in osteoarthritis. Lancet 2005;365:965-973. (Pubitemid 41071431)
113. Dieppe P: Developments in osteoarthritis. Rheumatology 2011;50:245-247.
114. Brandt KD, Radin EL, Dieppe PA, van de Putte L: Yet more evidence that osteoarthritis is not a cartilage disease. Ann Rheum Dis 2006;65:1261-1264. (Pubitemid 44620433)
115. Hunter DJ, Felson DT: Osteoarthritis. Brit Med J 2006;332:639-642B.
116. Creamer P, Hochberg MC: Osteoarthritis. Lancet 1997;350:503-509. (Pubitemid 27343314)
117. Simon WH, Green WT Jr: Experimental production of cartilage necrosis by cold injury: Failure to cause degenerative joint disease. Am J Pathol 1971;64:145-154.
118. Venn MF: Variation of chemical composition with age in human femoralhead cartilage. Ann Rheum Dis 1978;37:168-174. (Pubitemid 8371847)
119. Maroudas A: Balance between swelling pressure and collagen tension in normal and degenerate cartilage. Nature 1976;260:808-809.
120. Bollet AJ, Nance JL: Biochemical findings in normal and osteoarthritic articular cartilage. II. Chondroitin sulfate concentration and chain length water and ash content. J Clin Invest 1966;45:1170-1177.
121. Brocklehurst R, Bayliss MT, Maroudas A, Coysh HL, Freeman MA, Revell PA, Ali SY: The composition of normal and osteoarthritic articular cartilage from human knee joints. With special reference to unicompartmental replacement and osteotomy of the knee. J Bone Joint Surg Am 1984;66:95-106. (Pubitemid 14186735)
122. Grushko G, Schneiderman R, Maroudas A: Some biochemical and biophysical parameters for the study of the pathogenesis of osteoarthritis: A comparison between the processes of ageing and degeneration in human hip cartilage. Connect Tissue Res 1989;19:149-176.
123. Stockwell RA: Cartilage failure in osteoarthritis: Relevance of normal structure and function. A review. Clinical Anatomy 1991;4:161-191.
124. Bush PG, Hall AC: The volume and morphology of chondrocytes within nondegenerate and degenerate human articular cartilage. Osteoarthritis Cartilage 2003;11:242-251. (Pubitemid 36410876)
125. Bush PG, Hall AC: Passive osmotic properties of in situ human articular chondrocytes within non-degenerate and degenerate cartilage. J Cell Physiol 2005;204:309-319. (Pubitemid 40776834)
126. Bush PG, Hodkinson PD, Hamilton GL, Hall AC: Viability and volume of in situ bovine articular chondrocytes-changes following a single impact and effects of medium osmolarity. Osteoarthritis Cartilage 2005;13:54-65. (Pubitemid 40104264)
127. Maeno E, Takahashi N, Okada Y: Dysfunction of regulatory volume increase is a key component of apoptosis. Febs Letters 2006;580:6513-6517. (Pubitemid 44750945)
128. Goggs R, Carter SD, Schulze-Tanzil G, Shakibaei M, Mobasheri A: Apoptosis and the loss of chondrocyte survival signals contribute to articular cartilage degradation in osteoarthritis. Vet J 2003;166:140-158. (Pubitemid 37554969)
129. Mobasheri A: Role of chondrocyte death and hypocellularity in ageing human articular cartilage and the pathogenesis of osteoarthritis. Med Hypotheses 2002;58:193-197. (Pubitemid 34664889)
130. Murray DH, Bush PG, Brenkel IJ, Hall AC: Abnormal human chondrocyte morphology is related to increased levels of cell-associated il-1 beta and disruption to pericellular collagen type vi. J Orthop Res 2010;28:1507-1514.
131. Browning JA, Saunders K, Urban JPG, Wilkins RJ: The influence and interactions of hydrostatic and osmotic pressures on the intracellular milieu of chondrocytes. Biorheol 2004;41:299-308. (Pubitemid 39277087)
132. Pingguan-Murphy B, El-Azzeh M, Bader DL, Knight MM: Cyclic compression of chondrocytes modulates a purinergic calcium signalling pathway in a strain rate-and frequency-dependent manner. J Cell Physiol 2006;209:389-397. (Pubitemid 44484629)
133. Guilak F, Zell RA, Erickson GR, Grande DA, Rubin CT, McLeod KJ, Donahue HJ: Mechanically induced calcium waves in articular chondrocytes are inhibited by gadolinium and amiloride. J Orthop Res 1999;17:421-429. (Pubitemid 29275427)
134. Urban JPG, Hall AC, Gehl KA: Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J Cell Physiol 1993;154:262-270. (Pubitemid 23048006)
135. Hopewell B, Urban JPG: Adaptation of articular chondrocytes to changes in osmolality. Biorheol 2003;40:73-77.
136. Leipzig ND, Athanasiou KA: Static compression of single chondrocytes catabolically modifies single-cell gene expression. Biophys J 2008;94:2412-2422.
137. Buschmann MD, Gluzband YA, Grodzinsky AJ, Hunziker EB: Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. J Cell Sci 1995;108:1497-1508.
138. Mouw JK, Connelly JT, Wilson CG, Michael KE, Levenston ME: Dynamic compression regulates the expression and synthesis of chondrocyte-specific matrix molecules in bone marrow stromal cells. Stem Cells 2007;25:655-663. (Pubitemid 46354224)
139. Sah RLY, Kim YJ, Doong JYH, Grodzinsky AJ, Plaas AHK, Sandy JD: Biosynthetic response of cartilage explants to dynamic compression. J Orthop Res 1989;7:619-636. (Pubitemid 19208087)
140. Hall AC, Urban JPG, Gehl KA: The effects of hydrostatic-pressure on matrix synthesis in articular-cartilage. J Orthop Res 1991;9:1-10.
141. Karlsson C, Dehne T, Lindahl A, Brittberg M, Pruss A, Sittinger M, Ringe J: Genomewide expression profiling reveals new candidate genes associated with osteoarthritis. Osteoarthr Cartilage 2010;18:581-592.
142. Niemeyer MI, Cid LP, Barros LF, Sepulveda FV: Modulation of the twopore domain acid-sensitive K+ channel task-2 (kcnk5) by changes in cell volume. J Biol Chem 2001;276:43166-43174.
143. Patel AJ, Lazdunski M: The 2p-domain K+ channels: Role in apoptosis and tumorigenesis. Eur J Physiol Pflugers Archiv 2004;448:261-273. (Pubitemid 40895595)
144. Wehner F, Bohmer C, Heinzinger H, van den Boom F, Tinel H: The hypertonicityinduced Na+ conductance of rat hepatocytes: Physiological significance and molecular correlate. Cell Physiol Biochem 2000;10:335-340. (Pubitemid 32010735)
145. Trujillo E, Gonzalez T, Marin R, Martin-Vasallo P, Marples D, Mobasheri A: Human articular chondrocytes, synoviocytes and synovial microvessels express aquaporin water channels; upregulation of aqp1 in rheumatoid arthritis. Histol Histopathol 2004;19:435-444. (Pubitemid 38443905)
146. Hodgkin AL, Huxley AF: A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1952;117:500-544.
147. Detmers FJM, De Groot BL, Muller EM, Hinton A, Konings IBM, Sze M, Flitsch SL, Grubmuller H, Deen PMT: Quaternary ammonium compounds as water channel blockers-specificity, potency, and site of action. J Biol Chem 2006;281:14207-14214. (Pubitemid 43848348)
148. Garty H, Palmer LG: Epithelial sodium channels: Function, structure, and regulation. Physiol Rev 1997;77:359-396. (Pubitemid 27184343)
149. Alexander SPH, Mathie A, Peters JA: Guide to receptors and channels (grac), 3rd edition. Brit J Pharmacol 2008;153:S1-S209.