Extracellular osmolarity regulates matrix homeostasis in the intervertebral disc and articular cartilage: Evolving role of TonEBP

Matrix Biology

Volumn 40, Issue , 2014, Pages 10-16

  Johnson, Zariel I ^a   Shapiro, Irving M ^a   Risbud, Makarand V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Cartilage; Disc degeneration; Intervertebral disc; Osmoregulation; Proteoglycan rich matrix; TonEBP

Indexed keywords

AGGRECAN; BETA 1,3 GLUCORONOSYLTRANSFERASE; BINDING PROTEIN; COLLAGEN; COLLAGEN TYPE 2; HYPERTONIC SOLUTION; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR TONICITY RESPONSIVE ENHANCER BINDING PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; NFAT5 PROTEIN, HUMAN;

ARTICULAR CARTILAGE; CARTILAGE CELL; CATABOLISM; CELL FUNCTION; CELL SURVIVAL; DEGENERATIVE DISEASE; EXTRACELLULAR MATRIX; HOMEOSTASIS; HUMAN; HYDRATION; HYPEROSMOLARITY; IMMUNOCOMPETENT CELL; INFLAMMATION; INTERVERTEBRAL DISK; INTERVERTEBRAL DISK DEGENERATION; NONHUMAN; NUCLEUS PULPOSUS; OSMOLARITY; OSMOREGULATION; OSMOSIS; OSMOTIC PRESSURE; OSTEOARTHRITIS; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; REVIEW; SURVIVAL RATE; ADAPTATION; BIOMECHANICS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; BIOMECHANICAL PHENOMENA; CARTILAGE, ARTICULAR; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; INTERVERTEBRAL DISC; OSMOLAR CONCENTRATION; TRANSCRIPTION FACTORS;

EID: 84918554285     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.08.014     Document Type: Review

References (87)

1. Benfenati V., Caprini M., Dovizio M., Mylonakou M.N., Ferroni S., Ottersen O.P., Amiry-Moghaddam M. An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc. Natl. Acad. Sci. 2011, 108(6):2563-2568. (Feb 8). 10.1073/pnas.1012867108.
2. Boos N., Wallin A., Gbedegbegnon T., Aebi M., Boesch C. Quantitative MR imaging of lumbar intervertebral disks and vertebral bodies: influence of diurnal water content variations. Radiology 1993, 188:351-354. 10.1148/radiology.188.2.8327677.
3. Buxadé M., Lunazzi G., Minguillón J., Iborra S., Berga-Bolaños R., Del Val M., Aramburu J., López-Rodríguez C. Gene expression induced by Toll-like receptors in macrophages requires the transcription factor NFAT5. J. Exp. Med. 2012, 209:379-393. 10.1084/jem.20111569.
4. Cai Q., Ferraris J.D., Burg M.B. High NaCl increases TonEBP/OREBP mRNA and protein by stabilizing its mRNA. Am. J. Physiol. Ren. Physiol. 2005, 289:F803-F807. 10.1152/ajprenal.00448.2004.
5. Caron M.M.J., van der Windt A.E., Emans P.J., van Rhijn L.W., Jahr H., Welting T.J.M. Osmolarity determines the in vitro chondrogenic differentiation capacity of progenitor cells via nuclear factor of activated T-cells 5. Bone 2013, 53:94-102. 10.1016/j.bone.2012.11.032.
6. Chen J., Baer A.E., Paik P.Y., Yan W., Setton L.A. Matrix protein gene expression in intervertebral disc cells subjected to altered osmolarity. Biochem. Biophys. Res. Commun. 2002, 293:932-938. 10.1016/S0006-291X(02)00314-5.
7. Cheung C.Y., Ko B.C. NFAT5 in cellular adaptation to hypertonic stress - regulations and functional significance. J. Mol. Signal. 2013, 8:5. 10.1186/1750-2187-8-5.
8. Chou C.H., Lee C.H., Lu L.S., Song I.W., Chuang H.P., Kuo S.Y., Wu J.Y., Chen Y.T., Kraus V.B., Wu C.C., Lee M.T.M. Direct assessment of articular cartilage and underlying subchondral bone reveals a progressive gene expression change in human osteoarthritic knees. Osteoarthr. Cartil. 2013, 21:450-461. 10.1016/j.joca.2012.11.016.
9. Cs-Szabo G., Ragasa-San Juan D., Turumella V., Masuda K., Thonar E.J., An H.S. Changes in mRNA and protein levels of proteoglycans of the anulus fibrosus and nucleus pulposus during intervertebral disc degeneration. Spine (Phila Pa 1976) 2002, 27:2212-2219. 10.1097/01.BRS.0000029249.02864.5B.
10. Esensten J.H., Tsytsykova A.V., Lopez-Rodriguez C., Ligeiro F.A., Rao A., Goldfeld A.E. NFAT5 binds to the TNF promoter distinctly from NFATp, c, 3 and 4, and activates TNF transcription during hypertonic stress alone. Nucleic Acids Res. 2005, 33:3845-3854. 10.1093/nar/gki701.
11. Fenty M., Crescenzi R., Fry B., Squillante D., Turk D., Maurer P.M., Borthakur A. Novel imaging of the intervertebral disk and pain. Glob. Spine J. 2013, 3:127-132. 10.1055/s-0033-1347930.
12. Fujita N., Gogate S.S., Chiba K., Toyama Y., Shapiro I.M., Risbud M.V. Prolyl hydroxylase 3 (PHD3) modulates catabolic effects of tumor necrosis factor-α (TNF-α) on cells of the nucleus pulposus through co-activation of nuclear factor κB (NF-κB)/p65 signaling. J. Biol. Chem. 2012, 287:39942-39953. 10.1074/jbc.M112.375964.
13. Gajghate S., Hiyama A., Shah M., Sakai D., Anderson D.G., Shapiro I.M., Risbud M.V. Osmolarity and intracellular calcium regulate aquaporin2 expression through TonEBP in nucleus pulposus cells of the intervertebral disc. J. Bone Miner. Res. 2009, 24:992-1001. 10.1359/jbmr.090103.
14. Gallazzini M., Heussler G.E., Kunin M., Izumi Y., Burg M.B., Ferraris J.D. High NaCl-induced activation of CDK5 increases phosphorylation of the osmoprotective transcription factor TonEBP/OREBP at threonine 135, which contributes to its rapid nuclear localization. Mol. Biol. Cell 2011, 22(5):703-714. (Mar 1). 10.1091/mbc.E10-08-0681.
15. Garcia-Perez A., Burg M.B. Renal medullary organic osmolytes. Physiol. Rev. 1991, 71:1081-1115.
16. Gogate S.S., Fujita N., Skubutyte R., Shapiro I.M., Risbud M.V. Tonicity enhancer binding protein (TonEBP) and hypoxia-inducible factor (HIF) coordinate heat shock protein 70 (Hsp70) expression in hypoxic nucleus pulposus cells: role of Hsp70 in HIF-1α degradation. J. Bone Miner. Res. 2012, 27:1106-1117. 10.1002/jbmr.1571.
17. Haefeli M., Kalberer F., Saegesser D., Nerlich A.G., Boos N., Paesold G. The course of macroscopic degeneration in the human lumbar intervertebral disc. Spine (Phila Pa 1976) 2006, 31:1522-1531. 10.1097/01.brs.0000222032.52336.8e.
18. Halterman J.A., Kwon H.M., Wamhoff B.R. Tonicity-independent regulation of the osmosensitive transcription factor TonEBP (NFAT5). Am. J. Physiol. Cell Physiol. 2012, 302:C1-C8. 10.1152/ajpcell.00327.2011.
19. Handler J.S., Kwon H.M. Transcriptional regulation by changes in tonicity. Kidney Int. 2001, 60(2):408-411. (Aug).
20. Hani A.F.M., Kumar D., Malik A.S., Ahmad R.M.K.R., Razak R., Kiflie A. Non-invasive and in vivo assessment of osteoarthritic articular cartilage: a review on MRI investigations. Rheumatol. Int. 2014, 10.1007/s00296-014-3052-9.
21. Haschtmann D., Stoyanov J.V., Ferguson S.J. Influence of diurnal hyperosmotic loading on the metabolism and matrix gene expression of a whole-organ intervertebral disc model. J. Orthop. Res. 2006, 24:1957-1966. 10.1002/jor.20243.
22. Hiyama A., Gajghate S., Sakai D., Mochida J., Shapiro I.M., Risbud M.V. Activation of TonEBP by calcium controls {beta}1,3-glucuronosyltransferase-I expression, a key regulator of glycosaminoglycan synthesis in cells of the intervertebral disc. J. Biol. Chem. 2009, 284:9824-9834. 10.1074/jbc.M807081200.
23. Hiyama A., Gogate S.S., Gajghate S., Mochida J., Shapiro I.M., Risbud M.V. BMP-2 and TGF-beta stimulate expression of beta1,3-glucuronosyl transferase 1 (GlcAT-1) in nucleus pulposus cells through AP1, TonEBP, and Sp1: role of MAPKs. J. Bone Miner. Res. 2010, 25:1179-1190. 10.1359/jbmr.091202.
24. Im H.J., Muddasani P., Natarajan V., Schmid T.M., Block J.A., Davis F., van Wijnen A.J., Loeser R.F. Basic fibroblast growth factor stimulates matrix metalloproteinase-13 via the molecular cross-talk between the mitogen-activated protein kinases and protein kinase Cdelta pathways in human adult articular chondrocytes. J. Biol. Chem. 2007, 282:11110-11121. 10.1074/jbc.M609040200.
25. Ishihara H., Warensjo K., Roberts S., Urban J.P. Proteoglycan synthesis in the intervertebral disk nucleus: the role of extracellular osmolality. Am. J. Physiol. 1997, 272:C1499-C1506.
26. Jauliac S., López-Rodriguez C., Shaw L.M., Brown L.F., Rao A., Toker A. The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat. Cell Biol. 2002, 4(7):540-544. (Jul).
27. Katz J.N. Lumbar disc disorders and low-back pain: socioeconomic factors and consequences. J. Bone Joint Surg. Am. 2006, 88(Suppl. 2):21-24. 10.2106/JBJS.E.01273.
28. Kim H.A., Cho M.L., Choi H.Y., Yoon C.S., Jhun J.Y., Oh H.J., Kim H.Y. The catabolic pathway mediated by Toll-like receptors in human osteoarthritic chondrocytes. Arthritis Rheum. 2006, 54:2152-2163. 10.1002/art.21951.
29. Kim N.H., Hong B.K., Choi S.Y., Moo Kwon H., Cho C.S., Yi E.C., Kim W.U. Reactive oxygen species regulate context-dependent inhibition of NFAT5 target genes. Exp. Mol. Med. 2013, 45:e32. 10.1038/emm.2013.61.
30. Kojima R., Taniguchi H., Tsuzuki A., Nakamura K., Sakakura Y., Ito M. Hypertonicity-induced expression of monocyte chemoattractant protein-1 through a novel cis-acting element and MAPK signaling pathways. J. Immunol. 2010, 184:5253-5262. 10.4049/jimmunol.0901298.
31. Küper C., Beck F.X., Neuhofer W. NFAT5 contributes to osmolality-induced MCP-1 expression in mesothelial cells. Mediat. Inflamm. 2012, 2012:513015. 10.1155/2012/513015.
32. Lawrence J.S. Disc degeneration. Its frequency and relationship to symptoms. Ann. Rheum. Dis. 1969, 28:121-138.
33. Le Maitre C.L., Pockert A., Buttle D.J., Freemont A.J., Hoyland J.A. Matrix synthesis and degradation in human intervertebral disc degeneration. Biochem. Soc. Trans. 2007, 35:652-655. 10.1042/BST0350652.
34. Lee S.Do, Colla E., Sheen M.R., Na K.Y., Kwon H.M. Multiple domains of TonEBP cooperate to stimulate transcription in response to hypertonicity. J. Biol. Chem. 2003, 278:47571-47577. 10.1074/jbc.M308795200.
35. Lee A.S., Ellman M.B., Yan D., Kroin J.S., Cole B.J., van Wijnen A.J., Im H.-J. A current review of molecular mechanisms regarding osteoarthritis and pain. Gene 2013, 527:440-447. 10.1016/j.gene.2013.05.069.
36. Lefebvre V., Smits P. Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res. C Embryo Today 2005, 75:200-212. 10.1002/bdrc.20048.
37. Liu S.C., Hsu C.J., Fong Y.C., Chuang S.M., Tang C.H. CTGF induces monocyte chemoattractant protein-1 expression to enhance monocyte migration in human synovial fibroblasts. Biochim. Biophys. Acta 2013, 1833:1114-1124. 10.1016/j.bbamcr.2012.12.014.
38. Liu-Bryan R., Terkeltaub R. Chondrocyte innate immune myeloid differentiation factor 88-dependent signaling drives procatabolic effects of the endogenous Toll-like receptor 2/Toll-like receptor 4 ligands low molecular weight hyaluronan and high mobility group box chromosomal protein 1 in mice. Arthritis Rheum. 2010, 62(7):2004-2012. (Jul). 10.1002/art.27475.
39. López-Rodríguez C., Aramburu J., Jin L., Rakeman A.S., Michino M., Rao A. Bridging the NFAT and NF-kappaB families: NFAT5 dimerization regulates cytokine gene transcription in response to osmotic stress. Immunity 2001, 15:47-58.
40. López-Rodríguez C., Antos C.L., Shelton J.M., Richardson J.A., Lin F., Novobrantseva T.I., Bronson R.T., Igarashi P., Rao A., Olson E.N. Loss of NFAT5 results in renal atrophy and lack of tonicity-responsive gene expression. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2392-2397.
41. Maidhof R., Jacobsen T., Papatheodorou A., Chahine N.O. Inflammation induces irreversible biophysical changes in isolated nucleus pulposus cells. PLoS One 2014, 9:e99621. 10.1371/journal.pone.0099621.
42. Mak M.C., Lam K.M., Chan P.K., Lau Y.B., Tang W.H., Yeung P.K.K., Ko B.C.B., Chung S.M.S., Chung S.K. Embryonic lethality in mice lacking the nuclear factor of activated T cells 5 protein due to impaired cardiac development and function. PLoS One 2011, 6:e19186. 10.1371/journal.pone.0019186.
43. Miller J.A., Schmatz C., Schultz A.B. Lumbar disc degeneration: correlation with age, sex, and spine level in 600 autopsy specimens. Spine (Phila Pa 1976) 1988, 13:173-178.
44. Moeckel G.W., Zhang L., Chen X., Rossini M., Zent R., Pozzi A. Role of integrin alpha1beta1 in the regulation of renal medullary osmolyte concentration. Am. J. Physiol. Ren. Physiol. 2006, 290(1):F223-F231. (Jan).
45. Neidlinger-Wilke C., Mietsch A., Rinkler C., Wilke H.-J., Ignatius A., Urban J. Interactions of environmental conditions and mechanical loads have influence on matrix turnover by nucleus pulposus cells. J. Orthop. Res. 2012, 30:112-121. 10.1002/jor.21481.
46. Nguyen A.M., Johannessen W., Yoder J.H., Wheaton A.J., Vresilovic E.J., Borthakur A., Elliott D.M. Noninvasive quantification of human nucleus pulposus pressure with use of T1rho-weighted magnetic resonance imaging. J. Bone Joint Surg. Am. 2008, 90:796-802. 10.2106/JBJS.G.00667.
47. Palmer G.D., Chao Ph P.H., Raia F., Mauck R.L., Valhmu W.B., Hung C.T. Time-dependent aggrecan gene expression of articular chondrocytes in response to hyperosmotic loading. Osteoarthr. Cartil. 2001, 9:761-770. 10.1053/joca.2001.0473.
48. Peffers M.J., Milner P.I., Tew S.R., Clegg P.D. Regulation of SOX9 in normal and osteoarthritic equine articular chondrocytes by hyperosmotic loading. Osteoarthr. Cartil. 2010, 18:1502-1508. 10.1016/j.joca.2010.08.011.
49. Phillips K.L.E., Chiverton N., Michael A.L.R., Cole A.A., Breakwell L.M., Haddock G., Bunning R.A.D., Cross A.K., Le Maitre C.L. The cytokine and chemokine expression profile of nucleus pulposus cells: implications for degeneration and regeneration of the intervertebral disc. Arthritis Res. Ther. 2013, 15:R213. 10.1186/ar4408.
50. Rajan N.E., Bloom O., Maidhof R., Stetson N., Sherry B., Levine M., Chahine N.O. Toll-like receptor 4 (TLR4) expression and stimulation in a model of intervertebral disc inflammation and degeneration. Spine (Phila Pa 1976) 2013, 38:1343-1351. 10.1097/BRS.0b013e31826b71f4.
51. Risbud M.V., Shapiro I.M. Role of cytokines in intervertebral disc degeneration: pain and disc content. Nat. Rev. Rheumatol. 2014, 10:44-56. 10.1038/nrrheum.2013.160.
52. Roberts S., Urban J.P.G. Intervertebral discs. Encyclopedia of Occupational Health and Safety 2011, International Labor Organization, Geneva. H. Riihimäki, E. Viikari-Juntura (Eds.).
53. Roberts N., Hogg D., Whitehouse G.H., Dangerfield P. Quantitative analysis of diurnal variation in volume and water content of lumbar intervertebral discs. Clin. Anat. 1998, 11:1-8.
54. Roth I., Kwon H.M., Martin P., Fe E. Osmoprotective transcription factor NFAT5/TonEBP modulates nuclear factor-B activity. Physiol. C 2010, 21:3459-3474.
55. Roughley P.J., Lee E.R. Cartilage proteoglycans: structure and potential functions. Microsc. Res. Tech. 1994, 28:385-397. 10.1002/jemt.1070280505.
56. Scherer C., Pfisterer L., Wagner A., Hödebeck M., Cattaruzza M., Hecker M., Korff T. Arterial wall stress controls NFAT5 activity in vascular smooth muscle cells. J. Am. Heart Assoc. 2014, 3:e000626. 10.1161/JAHA.113.000626.
57. Schneiderman R., Keret D., Maroudas A. Effects of mechanical and osmotic pressure on the rate of glycosaminoglycan synthesis in the human adult femoral head cartilage: an in vitro study. J. Orthop. Res. 1986, 4:393-408. 10.1002/jor.1100040402.
58. Souza R.B., Kumar D., Calixto N., Singh J., Schooler J., Subburaj K., Li X., Link T.M., Majumdar S. Response of knee cartilage T1rho and T2 relaxation times to in vivo mechanical loading in individuals with and without knee osteoarthritis. Osteoarthr. Cartil. 2014, 10.1016/j.joca.2014.04.017.
59. Spillekom S., Smolders L.A., Grinwis G.C.M., Arkesteijn I.T.M., Ito K., Meij B.P., Tryfonidou M.A. Increased osmolarity and cell clustering preserve canine notochordal cell phenotype in culture. Tissue Eng. C. Methods 2014, 10.1089/ten.TEC.2013.0479.
60. Stroud J.C., Lopez-Rodriguez C., Rao A., Chen L. Structure of a TonEBP-DNA complex reveals DNA encircled by a transcription factor. Nat. Struct. Biol. 2002, 9:90-94. 10.1038/nsb749.
61. Takeno K., Kobayashi S., Negoro K., Uchida K., Miyazaki T., Yayama T., Shimada S., Baba H. Physical limitations to tissue engineering of intervertebral disc cells: effect of extracellular osmotic change on glycosaminoglycan production and cell metabolism. Laboratory investigation. J. Neurosurg. Spine 2007, 7:637-644. 10.3171/SPI-07/12/637.
62. Tew S.R., Peffers M.J., McKay T.R., Lowe E.T., Khan W.S., Hardingham T.E., Clegg P.D. Hyperosmolarity regulates SOX9 mRNA posttranscriptionally in human articular chondrocytes. Am. J. Physiol. Cell Physiol. 2009, 297:C898-C906. 10.1152/ajpcell.00571.2008.
63. Tew S.R., Vasieva O., Peffers M.J., Clegg P.D. Post-transcriptional gene regulation following exposure of osteoarthritic human articular chondrocytes to hyperosmotic conditions. Osteoarthr. Cartil. 2011, 19:1036-1046. 10.1016/j.joca.2011.04.015.
64. Tian Y., Yuan W., Fujita N., Wang J., Wang H., Shapiro I.M., Risbud M.V. Inflammatory cytokines associated with degenerative disc disease control aggrecanase-1 (ADAMTS-4) expression in nucleus pulposus cells through MAPK and NF-κB. Am. J. Pathol. 2013, 182:2310-2321. 10.1016/j.ajpath.2013.02.037.
65. Tong E.H.Y., Guo J.J., Huang A.L., Liu H., Hu C.D., Chung S.S.M., Ko B.C.B. Regulation of nucleocytoplasmic trafficking of transcription factor OREBP/TonEBP/NFAT5. J. Biol. Chem. 2006, 281:23870-23879. 10.1074/jbc.M602556200.
66. Tsai T.T., Danielson K.G., Guttapalli A., Oguz E., Albert T.J., Shapiro I.M., Risbud M.V. TonEBP/OREBP is a regulator of nucleus pulposus cell function and survival in the intervertebral disc. J. Biol. Chem. 2006, 281:25416-25424. 10.1074/jbc.M601969200.
67. Tsai T.T., Guttapalli A., Agrawal A., Albert T.J., Shapiro I.M., Risbud M.V. MEK/ERK signaling controls osmoregulation of nucleus pulposus cells of the intervertebral disc by transactivation of TonEBP/OREBP. J. Bone Miner. Res. 2007, 22:965-974. 10.1359/jbmr.070322.
68. Ueno M., Shen W.J., Patel S., Greenberg A.S., Azhar S., Kraemer F.B. Fat-specific protein 27 modulates nuclear factor of activated T cells 5 and the cellular response to stress. J. Lipid Res. 2013, 54:734-743. 10.1194/jlr.M033365.
69. Urban J.P. The chondrocyte: a cell under pressure. Br. J. Rheumatol. 1994, 33:901-908.
70. Urban J.P., Bayliss M.T. Regulation of proteoglycan synthesis rate in cartilage in vitro: influence of extracellular ionic composition. Biochim. Biophys. Acta 1989, 992:59-65.
71. Urban J.P., Hall A.C., Gehl K.A. Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J. Cell. Physiol. 1993, 154:262-270. 10.1002/jcp.1041540208.
72. Van der Windt A.E., Haak E., Das R.H.J., Kops N., Welting T.J.M., Caron M.M.J., van Til N.P., Verhaar J.A.N., Weinans H., Jahr H. Physiological tonicity improves human chondrogenic marker expression through nuclear factor of activated T-cells 5 in vitro. Arthritis Res. Ther. 2010, 12:R100. 10.1186/ar3031.
73. Van Dijk B., Potier E., Ito K. Culturing bovine nucleus pulposus explants by balancing medium osmolarity. Tissue Eng. C Methods 2011, 17:1089-1096. 10.1089/ten.TEC.2011.0215.
74. Van Dijk B.G.M., Potier E., Ito K. Long-term culture of bovine nucleus pulposus explants in a native environment. Spine J. 2013, 13:454-463. 10.1016/j.spinee.2012.12.006.
75. Verma P., Dalal K. ADAMTS-4 and ADAMTS-5: key enzymes in osteoarthritis. J. Cell. Biochem. 2011, 112:3507-3514. 10.1002/jcb.23298.
76. Wang J., Markova D., Anderson D.G., Zheng Z., Shapiro I.M., Risbud M.V. TNF-α and IL-1β promote a disintegrin-like and metalloprotease with thrombospondin type I motif-5-mediated aggrecan degradation through syndecan-4 in intervertebral disc. J. Biol. Chem. 2011, 286:39738-39749. 10.1074/jbc.M111.264549.
77. Wang J., Tian Y., Phillips K.L.E., Chiverton N., Haddock G., Bunning R.A., Cross A.K., Shapiro I.M., Le Maitre C.L., Risbud M.V. Tumor necrosis factor α- and interleukin-1β-dependent induction of CCL3 expression by nucleus pulposus cells promotes macrophage migration through CCR1. Arthritis Rheum. 2013, 65:832-842. 10.1002/art.37819.
78. Wang Q., Yang Y.Y., Niu H.J., Zhang W.J., Feng Q.J., Chen W.-F. An ultrasound study of altered hydration behaviour of proteoglycan-degraded articular cartilage. BMC Musculoskelet. Disord. 2013, 14:289. 10.1186/1471-2474-14-289.
79. Wei J., Richbourgh B., Jia T., Liu C. ADAMTS-12: a multifaced metalloproteinase in arthritis and inflammation. Mediat. Inflamm. 2014, 2014:649718. 10.1155/2014/649718.
80. Wheaton A.J., Borthakur A., Shapiro E.M., Regatte R.R., Akella S.V.S., Kneeland J.B., Reddy R. Proteoglycan loss in human knee cartilage: quantitation with sodium MR imaging-feasibility study. Radiology 2004, 231:900-905. 10.1148/radiol.2313030521.
81. Wiig H., Schröder A., Neuhofer W., Jantsch J., Kopp C., Karlsen T.V., Boschmann M., Goss J., Bry M., Rakova N., Dahlmann A., Brenner S., Tenstad O., Nurmi H., Mervaala E., Wagner H., Beck F.X., Müller D.N., Kerjaschki D., Luft F.C., Harrison D.G., Alitalo K., Titze J. Immune cells control skin lymphatic electrolyte homeostasis and blood pressure. J. Clin. Invest. 2013, 123:2803-2815. 10.1172/JCI60113.
82. Woo S.K., Dahl S.C., Handler J.S., Kwon H.M. Bidirectional regulation of tonicity-responsive enhancer binding protein in response to changes in tonicity. Am. J. Physiol. Ren. Physiol. 2000, 278:F1006-F1012.
83. Woo S.K., Lee S.Do, Na K.Y., Park W.K., Kwon H.M. TonEBP/NFAT5 stimulates transcription of HSP70 in response to hypertonicity. Mol. Cell. Biol. 2002, 22:5753-5760.
84. Wuertz K., Urban J.P.G., Klasen J., Ignatius A., Wilke H.J., Claes L., Neidlinger-Wilke C. Influence of extracellular osmolarity and mechanical stimulation on gene expression of intervertebral disc cells. J. Orthop. Res. 2007, 25:1513-1522. 10.1002/jor.20436.
85. Yancey P.H., Clark M.E., Hand S.C., Bowlus R.D., Somero G.N. Living with water stress: evolution of osmolyte systems. Science 1982, 217:1214-1222.
86. Yoon H.J., You S., Yoo S.A., Kim N.H., Kwon H.M., Yoon C.H., Cho C.S., Hwang D., Kim W.U. NF-AT5 is a critical regulator of inflammatory arthritis. Arthritis Rheum. 2011, 63:1843-1852. 10.1002/art.30229.
87. Zhou X., Wang H., Burg M.B., Ferraris J.D. Inhibitory phosphorylation of GSK-3β by AKT, PKA, and PI3K contributes to high NaCl-induced activation of the transcription factor NFAT5 (TonEBP/OREBP). Am. J. Physiol. Ren. Physiol. 2013, 304(7):F908-F917. (Apr 1). 10.1152/ajprenal.00591.2012.