RNA sequencing reveals a role of TonEBP transcription factor in regulation of pro-inflammatory genes in response to hyperosmolarity in healthy nucleus pulposus cells a homeostatic response?

Journal of Biological Chemistry

Volumn 291, Issue 52, 2016, Pages 26686-26697

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

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; DISEASES; ENZYME ACTIVITY; GENE EXPRESSION; GENES; MAMMALS; NITRIC OXIDE; PHYSIOLOGY; TISSUE HOMEOSTASIS; TRANSCRIPTION FACTORS;

BIOINFORMATIC ANALYSIS; ENHANCER BINDING PROTEINS; EXTRACELLULAR MATRICES; INTERVERTEBRAL DISCS; NITRIC-OXIDE SYNTHASE; PHYSIOLOGICAL ADAPTATIONS; SITE DIRECTED MUTAGENESIS; TUMOR NECROSIS FACTORS;

TRANSCRIPTION;

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TONICITY RESPONSIVE ENHANCER BINDING PROTEIN; UNCLASSIFIED DRUG; AUTACOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR NFAT;

ARTICLE; BINDING AFFINITY; CCL2 GENE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE; GENETIC TRANSCRIPTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IL6 GENE; NOS2 GENE; NUCLEUS PULPOSUS; OSMOSIS; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA SEQUENCE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; TNF GENE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; INTERVERTEBRAL DISK; KNOCKOUT MOUSE; METABOLISM; MOUSE; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PROCEDURES; RAT; SIGNAL TRANSDUCTION;

ANIMALS; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMEOSTASIS; INFLAMMATION MEDIATORS; INTERVERTEBRAL DISC; MICE; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; NUCLEUS PULPOSUS; ORGAN CULTURE TECHNIQUES; OSMOSIS; PROMOTER REGIONS, GENETIC; RATS; SIGNAL TRANSDUCTION;

EID: 85007342640     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.757732     Document Type: Article

References (49)

1. Inoue, N., and Espinoza Orías, A. A. (2011) Biomechanics of intervertebral disk degeneration. Orthop. Clin. North Am. 42, 487-499, vii
2. Kiani, C., Chen, L., Wu, Y. J., Yee, A. J., and Yang, B. B. (2002) Structure and function of aggrecan. Cell Res. 12, 19-32
3. Johnson, Z. I., Shapiro, I. M., and Risbud, M. V. (2014) Extracellular osmolarity regulates matrix homeostasis in the intervertebral disc and articular cartilage: Evolving role of TonEBP. Matrix Biol. 40, 10-16
4. Eyre, D. R., and Muir, H. (1977) Quantitative analysis of types I and II collagens in human intervertebral discs at various ages. Biochim. Biophys. Acta 492, 29-42
5. Borthakur, A., Maurer, P. M., Fenty, M., Wang, C., Berger, R., Yoder, J., Balderston, R. A., and Elliott, D. M. (2011) T1ρ magnetic resonance imaging and discography pressure as novel biomarkers for disc degeneration and low back pain. Spine 36, 2190-2196
6. Matsumura, Y., Kasai, Y., Obata, H., Matsushima, S., Inaba, T., and Uchida, A. (2009) Changes in water content of intervertebral discs and paravertebral muscles before and after bed rest. J. Orthop. Sci. 14, 45-50
7. Burg, M. B., Kwon, E. D., and Kültz, D. (1997) Regulation of gene expression by hypertonicity. Annu. Rev. Physiol. 59, 437-455
8. Chen, S., Grigsby, C. L., Law, C. S., Ni, X., Nekrep, N., Olsen, K., Humphreys, M. H., and Gardner, D. G. (2009) Tonicity-dependent induction of Sgk1 expression has a potential role in dehydration-induced natriuresis in rodents. J. Clin. Invest. 119, 1647-1658
9. Lanaspa, M. A., Andres-Hernando, A., Li, N., Rivard, C. J., Cicerchi, C., Roncal-Jimenez, C., Schrier, R. W., and Berl, T. (2010) The expression of aquaporin-1 in the medulla of the kidney is dependent on the transcription factor associated with hypertonicity, TonEBP. J. Biol. Chem. 285, 31694-31703
10. Hollborn, M., Vogler, S., Reichenbach, A., Wiedemann, P., Bringmann, A., and Kohen, L. (2015) Regulation of the hyperosmotic induction of aquaporin 5 and VEGF in retinal pigment epithelial cells: involvement of NFAT5. Mol. Vis. 21, 360-377
11. Lee, S. D., Choi, S. Y., Lim, S. W., Lamitina, S. T., Ho, S. N., Go, W. Y., and Kwon, H. M. (2011) TonEBP stimulates multiple cellular pathways for adaptation to hypertonic stress: organic osmolyte-dependent and-independent pathways. Am. J. Physiol. Renal Physiol. 300, F707-F715
12. Kojima, R., Taniguchi, H., Tsuzuki, A., Nakamura, K., Sakakura, Y., and Ito, M. (2010) Hypertonicity-induced expression of monocyte chemoattractant protein-1 through a novel cis-acting element andMAPKsignaling pathways. J. Immunol. 184, 5253-5262
13. Esensten, J. H., Tsytsykova, A. V., Lopez-Rodriguez, C., Ligeiro, F. A., Rao, A., and Goldfeld, A. E. (2005) NFAT5 binds to the TNF promoter distinctly from NFATp, c, 3 and 4, and activates TNF transcription during hypertonic stress alone. Nucleic Acids Res. 33, 3845-3854
14. López-Rodríguez, C., Aramburu, J., Jin, L., Rakeman, A. S., Michino, M., and Rao, A. (2001) Bridging the NFAT and NF-κB families: NFAT5 dimerization regulates cytokine gene transcription in response to osmotic stress. Immunity 15, 47-58
15. Buxadé, M., Lunazzi, G., Minguillón, J., Iborra, S., Berga-Bolaños, R., Del Val, M., Aramburu, J., and López-Rodríguez, C. (2012) Gene expression induced by Toll-like receptors in macrophages requires the transcription factor NFAT5. J. Exp. Med. 209, 379-393
16. Kim, N.-H., Hong, B.-K., Choi, S. Y., Moo Kwon, H., Cho, C.-S., Yi, E. C., and Kim, W.-U. (2013) Reactive oxygen species regulate context-dependent inhibition of NFAT5 target genes. Exp. Mol. Med. 45, e32
17. Tsai, T.-T., Danielson, K. G., Guttapalli, A., Oguz, E., Albert, T. J., Shapiro, I. M., and Risbud, M. V., (2006) TonEBP/OREBP is a regulator of nucleus pulposus cell function and survival in the intervertebral disc. J. Biol. Chem. 281, 25416-25524
18. Hiyama, A., Gajghate, S., Sakai, D., Mochida, J., Shapiro, I. M., and Risbud, M. V. (2009) Activation of TonEBP by calcium controls β1,3-glucuronosyltransferase-I expression, a key regulator of glycosaminoglycan synthesis in cells of the intervertebral disc. J. Biol. Chem. 284, 9824-9834
19. 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., and Jahr, H. (2010) Physiological tonicity improves human chondrogenic marker expression through nuclear factor of activated T-cells 5 in vitro. Arthritis Res. Ther. 12, R100
20. Go, W. Y., Liu, X., Roti, M. A., Liu, F., and Ho, S. N. (2004) NFAT5/ TonEBP mutant mice define osmotic stress as a critical feature of the lymphoid microenvironment. Proc. Natl. Acad. Sci. U.S.A. 101, 10673-10678
21. Gajghate, S., Hiyama, A., Shah, M., Sakai, D., Anderson, D. G., Shapiro, I. M., and Risbud, M. V. (2009) Osmolarity and intracellular calcium regulate aquaporin2 expression through TonEBP in nucleus pulposus cells of the intervertebral disc. J. Bone Miner. Res. 24, 992-1001
22. Tsai, T.-T., Guttapalli, A., Agrawal, A., Albert, T. J., Shapiro, I. M., and Risbud, M. V. (2007) MEK/ERK signaling controls osmoregulation of nucleus pulposus cells of the intervertebral disc by transactivation of TonEBP/OREBP. J. Bone Miner. Res. 22, 965-974
23. Hiyama, A., Gogate, S. S., Gajghate, S., Mochida, J., Shapiro, I. M., and Risbud, M. V. (2010) 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. 25, 1179-1190
24. Ueno, M., Shen, W.-J., Patel, S., Greenberg, A. S., Azhar, S., and Kraemer, F. B. (2013) Fat-specific protein 27 modulates nuclear factor of activated T cells 5 and the cellular response to stress. J. Lipid Res. 54, 734-743
25. Huang, W., Liu, H., Wang, T., Zhang, T., Kuang, J., Luo, Y., Chung, S. S. M., Yuan, L., and Yang, J. Y. (2011) Tonicity-responsive microRNAs contribute to the maximal induction of osmoregulatory transcription factor OREBP in response to high-NaCl hypertonicity. Nucleic Acids Res. 39, 475-485
26. Roth, I., Leroy, V., Kwon, H. M., Martin, P.-Y., Féraille, E., and Hasler, U. (2010) Osmoprotective transcription factor NFAT5/TonEBP modulates nuclear factor-κB activity. Mol. Biol. Cell. 21, 3459-3474
27. Wright, F. L., Gamboni, F., Moore, E. E., Nydam, T. L., Mitra, S., Silliman, C. C., and Banerjee, A. (2014) Hyperosmolarity invokes distinct anti-inflammatory mechanisms in pulmonary epithelial cells: evidence from signaling and transcription layers. PLoS ONE. 9:e114129
28. Lee, H. H., Sanada, S., An, S. M., Ye, B. J., Lee, J. H., Seo, Y.-K., Lee, C., Lee-Kwon, W., Küper, C., Neuhofer, W., Choi, S. Y., and Kwon, H. M. (2016) LPS-induced NFκB enhanceosome requires TonEBP/NFAT5 without DNA binding. Sci. Rep. 6, 24921
29. Satomi, K., Hirabayashi, K., Toyama, Y., and Fujimura, Y. (1992) A clinical study of degenerative spondylolisthesis: radiographic analysis and choice of treatment. Spine 17, 1329-1336
30. Risbud, M. V., and Shapiro, I. M. (2014) Role of cytokines in intervertebral disc degeneration: pain and disc content. Nat. Rev. Rheumatol. 10, 44-56
31. Schleich, C., Müller-Lutz, A., Matuschke, F., Sewerin, P., Sengewein, R., Schmitt, B., Ostendorf, B., Wittsack, H.-J., Stanke, K., Antoch, G., and Miese, F. (2015) Glycosaminoglycan chemical exchange saturation transfer of lumbar intervertebral discs in patients with spondyloarthritis. J. Magn. Reson. Imaging. 42, 1057-1063
32. Watanabe, T., Kato, S., Sato, K., and Nagata, K. (2005) Nitric oxide regulation system in degenerative lumbar disease. Kurume Med. J. 52, 39-47
33. 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., and Le Maitre, C. L. (2013) The cytokine and chemokine expression profile of nucleus pulposus cells: implications for degeneration and regeneration of the intervertebral disc. Arthritis Res. Ther. 15, R213
34. Altun, I. (2016) Cytokine profile in degenerated painful intervertebral disc: variability with respect to duration of symptoms and type of disease. Spine J. 16, 857-861
35. Dudek, M., Yang, N., Ruckshanthi, J. P., Williams, J., Borysiewicz, E., Wang, P., Adamson, A., Li, J., Bateman, J. F., White, M. R., Boot-Handford, R. P., Hoyland, J. A., and Meng, Q.-J. (2016) The intervertebral disc contains intrinsic circadian clocks that are regulated by age and cytokines and linked to degeneration. Ann. Rheum. Dis. 10.1136/annrheumdis-2016-209428
36. Suyama, K., Silagi, E. S., Choi, H., Sakabe, K., Mochida, J., Shapiro, I. M., and Risbud, M. V. (2016) Circadian factors BMAL1 and RORα control HIF-1α transcriptional activity in nucleus pulposus cells: implications in maintenance of intervertebral disc health. Oncotarget 7, 23056-23071
37. Fang W. B, Jokar, I., Zou, A., Lambert, D., Dendukuri, P., and Cheng, N. (2012) CCL2/CCR2 chemokine signaling coordinates survival and motility of breast cancer cells through Smad3 protein-and p42/44 mitogenactivated protein kinase (MAPK)-dependent mechanisms. J. Biol. Chem. 287, 36593-36608
38. Chen, Q., Sun, W., Liao, Y., Zeng, H., Shan, L., Yin, F., Wang, Z., Zhou, Z., Hua, Y., and Cai, Z. (2015) Monocyte chemotactic protein-1 promotes the proliferation and invasion of osteosarcoma cells and upregulates the expression of AKT. Mol. Med. Rep. 12, 219-225
39. Ji, W.-T., Chen, H.-R., Lin, C.-H., Lee, J.-W., and Lee, C.-C. (2014) Monocyte chemotactic protein 1 (MCP-1) modulates pro-survival signaling to promote progression of head and neck squamous cell carcinoma. PLoS ONE 9, e88952
40. Risbud, M. V., Guttapalli, A., Albert, T. J., and Shapiro, I. M. (2005) Hypoxia activates MAPK activity in rat nucleus pulposus cells: regulation of integrin expression and cell survival. Spine 30, 2503-2509
41. Risbud, M. V., Fertala, J., Vresilovic, E. J., Albert, T. J., and Shapiro, I. M. (2005) Nucleus pulposus cells upregulate PI3K/Akt and MEK/ERK signaling pathways under hypoxic conditions and resist apoptosis induced by serum withdrawal. Spine 30, 882-889
42. Cheng, C.-C., Uchiyama, Y., Hiyama, A., Gajghate, S., Shapiro, I. M., and Risbud, M. V. (2009) PI3K/AKT regulates aggrecan gene expression by modulating Sox9 expression and activity in nucleus pulposus cells of the intervertebral disc. J. Cell. Physiol. 221, 668-676
43. Li, Z., Shen, J., Wu, W. K. K., Yu, X., Liang, J., Qiu, G., and Liu, J. (2012) Leptin induces cyclin D1 expression and proliferation of human nucleus pulposus cells via JAK/STAT, PI3K/Akt and MEK/ERK pathways. PLoS ONE 7, e53176
44. Risbud, M. V., Guttapalli, A., Stokes, D. G., Hawkins, D., Danielson, K. G., Schaer, T. P., Albert, T. J., and Shapiro, I. M. (2006) Nucleus pulposus cells express HIF-1α under normoxic culture conditions: a metabolic adaptation to the intervertebral disc microenvironment. J. Cell. Biochem. 98, 152-159
45. Zenker, S., Panteleev-Ivlev, J., Wirtz, S., Kishimoto, T., Waldner, M. J., Ksionda, O., Tybulewicz, V. L. J., Neurath, M. F., and Atreya, I. (2014) A key regulatory role for Vav1 in controlling lipopolysaccharide endotoxemia via macrophage-derived IL-6. J. Immunol. 192, 2830-2836
46. Ito, T., Fujio, Y., Hirata, M., Takatani, T., Matsuda, T., Muraoka, S., Takahashi, K., and Azuma, J. (2004) Expression of taurine transporter is regulated through the TonE (tonicity-responsive element)/TonEBP (TonEbinding protein) pathway and contributes to cytoprotection in HepG2 cells. Biochem. J. 382, 177-182
47. Fu, J., and Taubman, M. B. (2010) Prolyl hydroxylase EGLN3 regulates skeletal myoblast differentiation through an NF-κB-dependent pathway. J. Biol. Chem. 285, 8927-8935
48. Lowenstein, C. J., Alley, E. W., Raval, P., Snowman, A. M., Snyder, S. H., Russell, S. W., and Murphy, W. J. (1993) Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon and lipopolysaccharide. Proc. Natl. Acad. Sci. U.S.A. 90, 9730-9734
49. Sanjabi, S., Williams, K. J., Saccani, S., Zhou, L., Hoffmann, A., Ghosh, G., Gerondakis, S., Natoli, G., and Smale, S. T. (2005) A c-Rel subdomain responsible for enhanced DNA-binding affinity and selective gene activation. Genes Dev. 19, 2138-2151