TGFβ regulates Galectin-3 expression through canonical Smad3 signaling pathway in nucleus pulposus cells: Implications in intervertebral disc degeneration

Matrix Biology

Volumn 50, Issue , 2016, Pages 39-52

  Tian, Ye ^a,b   Yuan, Wen ^b   Li, Jun ^a,b   Wang, Hua ^a,c   Hunt, Maxwell G ^a   Liu, Chao ^a,d   Shapiro, Irving M ^a   Risbud, Makarand V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^d SHANGHAI FIRST PEOPLE S HOSPITAL   (China)

Author keywords

Disc degeneration; Galectin 3; Intervertebral disc; Nucleus pulposus; Smad3; TGF

Indexed keywords

GALECTIN 3; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; GENE DELETION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERVERTEBRAL DISK DEGENERATION; NUCLEUS PULPOSUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; BINDING SITE; CELL CULTURE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROMOTER REGION; RAT;

ANIMALS; BINDING SITES; CELLS, CULTURED; GALECTIN 3; GENE EXPRESSION REGULATION; HUMANS; INTERVERTEBRAL DISC DEGENERATION; NUCLEUS PULPOSUS; PROMOTER REGIONS, GENETIC; RATS; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84949666908     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2015.11.008     Document Type: Article

References (46)

1. Feng H., Danfelter M., Stromqvist B., Heinegard D. Extracellular matrix in disc degeneration. J. Bone Joint Surg. Am. 2006, 88(Suppl. 2):25-29.
2. Setton L.A., Chen J. Mechanobiology of the intervertebral disc and relevance to disc degeneration. J. Bone Joint Surg. Am. 2006, 88(Suppl. 2):52-57.
3. Ng L., Grodzinsky A.J., Patwari P., Sandy J., Plaas A., Ortiz C. Individual cartilage aggrecan macromolecules and their constituent glycosaminoglycans visualized via atomic force microscopy. J. Struct. Biol. 2003, 143:242-257.
4. Stemple D.L. Structure and function of the notochord: an essential organ for chordate development. Development 2005, 132:2503-2512.
5. Götz W., Kasper M., Miosge N., Hughes R.C. Detection and distribution of the carbohydrate binding protein Galectin-3 in human notochord, intervertebral disc and chordoma. Differentiation 1997, 62:149-157.
6. Oguz E., Tsai T.-T., Di Martino A., Guttapalli A., Albert T.J., Shapiro I.M., Risbud M.V. Galectin-3 expression in the intervertebral disc: a useful marker of the notochord phenotype?. Spine (Phila Pa 1976) 2007, 32:9-16.
7. Woo H.J., Shaw L.M., Messier J.M., Mercurio A.M. The major non-integrin laminin binding protein of macrophages is identical to carbohydrate binding protein 35 (Mac-2). J. Biol. Chem. 1990, 265:7097-7099.
8. Sato S., Hughes R.C. Binding specificity of a baby hamster kidney lectin for H type I and II chains, polylactosamine glycans, and appropriately glycosylated forms of laminin and fibronectin. J. Biol. Chem. 1992, 267:6983-6990.
9. Hikita C., Vijayakumar S., Takito J., Erdjument-Bromage H., Tempst P., Al-Awqati Q. Induction of terminal differentiation in epithelial cells requires polymerization of hensin by Galectin 3. J. Cell Biol. 2000, 151:1235-1246.
10. Ochieng J., Warfield P., Green-Jarvis B., Fentie I. Galectin-3 regulates the adhesive interaction between breast carcinoma cells and elastin. J. Cell. Biochem. 1999, 75:505-514.
11. Ochieng J., Warfield P., L.-B.M.L. Regulation of cellular adhesion to extracellular matrix proteins by Galectin-3. Biochem. Biophys. Res. Commun. 1998, 246(3):788-791.
12. Bao Q., Hughes R.C. Galectin-3 expression and effects on cyst enlargement and tubulogenesis in kidney epithelial MDCK cells cultured in three-dimensional matrices in vitro. J. Cell Sci. 1995, 108:2791-2800.
13. Liu F.T. S-type mammalian lectins in allergic inflammation. Immunol. Today 1993, 14:486-490.
14. Ohshima S., Kuchen S., Seemayer C.A., Kyburz D., Hirt A., Klinzing S., Michel B.A., Gay R.E., Liu F.T., Gay S., Neidhart M. Galectin 3 and its binding protein in rheumatoid arthritis. Arthritis Rheum. 2003, 48:2788-2795.
15. Boileau C., Poirier F., Pelletier J.-P., Guévremont M., Duval N., Martel-Pelletier J., Reboul P. Intracellular localisation of Galectin-3 has a protective role in chondrocyte survival. Ann. Rheum. Dis. 2008, 67:175-181.
16. Ezzat M.H.M., El-Gammasy T.M.A., Shaheen K.Y.A., Osman A.O.Y. Elevated production of Galectin-3 is correlated with juvenile idiopathic arthritis disease activity, severity, and progression. Int. J. Rheum. Dis. 2011, 14:345-352.
17. Forsman H., Islander U., Andréasson E., Andersson A., Onnheim K., Karlström A., Sävman K., Magnusson M., Brown K.L., Karlsson A. Galectin 3 aggravates joint inflammation and destruction in antigen-induced arthritis. Arthritis Rheum. 2011, 63:445-454.
18. Stock M., Schäfer H., Stricker S., Gross G., Mundlos S., Otto F. Expression of Galectin-3 in skeletal tissues is controlled by Runx2. J. Biol. Chem. 2003, 278:17360-17367.
19. Costessi A., Pines A., D'Andrea P., Romanello M., Damante G., Cesaratto L., Quadrifoglio F., Moro L., Tell G. Extracellular nucleotides activate Runx2 in the osteoblast-like HOBIT cell line: a possible molecular link between mechanical stress and osteoblasts' response. Bone 2005, 36:418-432.
20. Zeng Y., Danielson K.G., Albert T.J., Shapiro I.M., Risbud M.V. HIF-1 alpha is a regulator of Galectin-3 expression in the intervertebral disc. J. Bone Miner. Res. 2007, 22:1851-1861.
21. Tran C.M., Markova D., Smith H.E., Susarla B., Ponnappan R.K., Anderson D.G., Symes A., Shapiro I.M., Risbud M.V. Regulation of CCN2/connective tissue growth factor expression in the nucleus pulposus of the intervertebral disc: role of Smad and activator protein 1 signaling. Arthritis Rheum. 2010, 62:1983-1992.
22. Yokoi H., Mukoyama M., Nagae T., Mori K., Suganami T., Sawai K., Yoshioka T., Koshikawa M., Nishida T., Takigawa M., Sugawara A., Nakao K. Reduction in connective tissue growth factor by antisense treatment ameliorates renal tubulointerstitial fibrosis. J. Am. Soc. Nephrol. 2004, 15:1430-1440.
23. Lee S., Moon C.S., Sul D., Lee J., Bae M., Hong Y., Lee M., Choi S., Derby R., Kim B.J., Kim J., Yoon J.S., Wolfer L., Kim J., Wang J., Hwang S.W., Lee S.H. Comparison of growth factor and cytokine expression in patients with degenerated disc disease and herniated nucleus pulposus. Clin. Biochem. 2009, 42:1504-1511.
24. Risbud M.V., Di Martino A., Guttapalli A., Seghatoleslami R., Denaro V., Vaccaro A.R., Albert T.J., Shapiro I.M. Toward an optimum system for intervertebral disc organ culture: TGF-β3 enhances nucleus pulposus and anulus fibrosus survival and function through modulation of TGF-beta-R expression and ERK signaling. Spine (Phila Pa 1976) 2006, 31:884-890.
25. Hiyama A., Gogate S.S., Gajghate S., Mochida J., Shapiro I.M., Risbud M.V. BMP-2 and TGF-β stimulate expression of β1,3-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.
26. Tran C.M., Fujita N., Huang B.-L., Ong J.R., Lyons K.M., Shapiro I.M., Risbud M.V. Hypoxia-inducible factor (HIF)-1α and CCN2 form a regulatory circuit in hypoxic nucleus pulposus cells: CCN2 suppresses HIF-1α level and transcriptional activity. J. Biol. Chem. 2013, 288:12654-12666.
27. Tran C.M., Schoepflin Z.R., Markova D.Z., Kepler C.K., Anderson D.G., Shapiro I.M., Risbud M.V. CCN2 suppresses catabolic effects of interleukin-1β through α5β1 and αVβ3 integrins in nucleus pulposus cells: implications in intervertebral disc degeneration. J. Biol. Chem. 2014, 289:7374-7387.
28. Tran C.M., Shapiro I.M., Risbud M.V. Molecular regulation of CCN2 in the intervertebral disc: lessons learned from other connective tissues. Matrix Biol. 2013, 32:298-306.
29. Wan Z.-Y., Sun Z., Song F., Chen Y.-F., Zhang W.-L., Wang H.-Q., Luo Z.-J. Downregulated interleukin 37 expression associated with aggravation of intervertebral disc degeneration. Int. J. Clin. Exp. Pathol. 2014, 7:656-662.
30. Hayashi H., Abdollah S., Qiu Y., Cai J., Xu Y.Y., Grinnell B.W., Richardson M.A., Topper J.N., Gimbrone M.A., Wrana J.L., Falb D. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 1997, 89:1165-1173.
31. Kavsak P., Rasmussen R.K., Causing C.G., Bonni S., Zhu H., Thomsen G.H., Wrana J.L. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell 2000, 6:1365-1375.
32. Zhang S., Fei T., Zhang L., Zhang R., Chen F., Ning Y., Han Y., Feng X.-H., Meng A., Chen Y.-G. Smad7 antagonizes transforming growth factor beta signaling in the nucleus by interfering with functional Smad-DNA complex formation. Mol. Cell. Biol. 2007, 27:4488-4499.
33. Wu Q., Wang J., Skubutyte R., Kepler C.K., Huang Z., Anderson D.G., Shapiro I.M., Risbud M.V. Smad3 controls β-1,3-glucuronosyltransferase 1 expression in rat nucleus pulposus cells: implications of dysregulated expression in disc disease. Arthritis Rheum. 2012, 64:3324-3333.
34. Akahani S., Nangia-Makker P., Inohara H., Kim H.R.C., Raz A. Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res. 1997, 57:5272-5276.
35. Fukumori T., Takenaka Y., Oka N., Yoshii T., Hogan V., Inohara H., Kanayama H.O., Kim H.R.C., Raz A. Endogenous Galectin-3 determines the routing of CD95 apoptotic signaling pathways. Cancer Res. 2004, 64:3376-3379.
36. Oka N., Nakahara S., Takenaka Y., Fukumori T., Hogan V., Kanayama H.-O., Yanagawa T., Raz A. Galectin-3 inhibits tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by activating Akt in human bladder carcinoma cells. Cancer Res. 2005, 65:7546-7553.
37. Lapis K., Tímár J. Role of elastin-matrix interactions in tumor progression. Semin. Cancer Biol. 2002, 12(3):209-217.
38. Furtak V., Hatcher F., Ochieng J. Galectin-3 mediates the endocytosis of β-1 integrins by breast carcinoma cells. Biochem. Biophys. Res. Commun. 2001, 289:845-850.
39. Sasaki T., Brakebusch C., Engel J., Timpl R. Mac-2 binding protein is a cell-adhesive protein of the extracellular matrix which self-assembles into ring-like structures and binds β1 integrins, collagens and fibronectin. EMBO J. 1998, 17:1606-1613.
40. Filer A., Bik M., Parsonage G.N., Fitton J., Trebilcock E., Howlett K., Cook M., Raza K., Simmons D.L., Thomas A.M.C., Salmon M., Scheel-Toellner D., Lord J.M., Rabinovich G.A., Buckley C.D. Galectin 3 induces a distinctive pattern of cytokine and chemokine production in rheumatoid synovial fibroblasts via selective signaling pathways. Arthritis Rheum. 2009, 60:1604-1614.
41. Risbud M.V., Shapiro I.M. Role of cytokines in intervertebral disc degeneration: pain and disc content. Nat. Rev. Rheumatol. 2014, 10:44-56.
42. Wang X., Wang H., Yang H., Li J., Cai Q., Shapiro I.M., Risbud M.V. TNF-α and IL-1β dependent MMP-3 expression in nucleus pulposus cells requires cooperative signaling via Syndecan4 and MAPK-NF-κB axis: implications in inflammatory disc disease. Am. J. Pathol. 2014, 184:2560-2572.
43. 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.
44. Quero L., Klawitter M., Schmaus A., Rothley M., Sleeman J., Tiaden A.N., Klasen J., Boos N., Hottiger M.O., Wuertz K., Richards P.J. Hyaluronic acid fragments enhance the inflammatory and catabolic response in human intervertebral disc cells through modulation of toll-like receptor 2 signalling pathways. Arthritis Res. Ther. 2013, 15:R94.
45. Risbud M.V., Guttapalli A., Stokes D.G., Hawkins D., Danielson K.G., Schaer T.P., Albert T.J., Shapiro I.M. Nucleus pulposus cells express HIF-1alpha under normoxic culture conditions: a metabolic adaptation to the intervertebral disc microenvironment. J. Cell. Biochem. 2006, 98:152-159.
46. Pfirrmann C.W., Metzdorf A., Zanetti M., Hodler J., Boos N. Magnetic resonance classification of lumbar intervertebral disc degeneration. Spine (Phila Pa 1976) 2001, 26:1873-1878.