RelB/p50 complexes regulate cytokine-induced YKL-40 expression

Journal of Immunology

Volumn 194, Issue 6, 2015, Pages 2862-2870

  Bhardwaj, Reetika ^a   Yester, Jessie W ^a   Singh, Sandeep K ^a   Biswas, Debolina D ^a   Surace, Michael J ^a   Waters, Michael R ^a   Hauser, Kurt F ^a   Yao, Zhenqiang ^b   Boyce, Brendan F ^b   Kordula, Tomasz ^a,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 6; ONCOSTATIN M; PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; UNCLASSIFIED DRUG; YKL 40 PROTEIN; ADIPOCYTOKINE; CHI3L1 PROTEIN, HUMAN; CHITINASE 3-LIKE 1, MOUSE; GLYCOPROTEIN; LECTIN; MULTIPROTEIN COMPLEX; PROTEIN BINDING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; ASTROCYTE; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; GENETICS; INFLAMMATION; METABOLISM; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSGENIC MOUSE; TUMOR CELL LINE; WESTERN BLOTTING;

ADIPOKINES; ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CELL LINE, TUMOR; CELLS, CULTURED; CYTOKINES; FEMALE; GENE EXPRESSION; GLYCOPROTEINS; HUMANS; INFLAMMATION; INTERLEUKIN-1; INTERLEUKIN-6; LECTINS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MULTIPROTEIN COMPLEXES; NF-KAPPA B P50 SUBUNIT; ONCOSTATIN M; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELB;

EID: 84924559911     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400874     Document Type: Article

References (64)

1. Roslind, A., and J. S. Johansen. 2009. YKL-40: a novel marker shared by chronic inflammation and oncogenic transformation. Methods Mol. Biol. 511: 159.184.
2. Kawamura, K., T. Shibata, O. Saget, D. Peel, and P. J. Bryant. 1999. A new family of growth factors produced by the fat body and active on Drosophila imaginal disc cells. Development 126: 211.219.
3. Hakala, B. E., C. White, and A. D. Recklies. 1993. Human cartilage gp-39, a major secretory product of articular chondrocytes and synovial cells, is a mammalian member of a chitinase protein family. J. Biol. Chem. 268: 25803. 25810.
4. De Ceuninck, F., S. Gaufillier, A. Bonnaud, M. Sabatini, C. Lesur, and P. Pastoureau. 2001. YKL-40 (cartilage gp-39) induces proliferative events in cultured chondrocytes and synoviocytes and increases glycosaminoglycan synthesis in chondrocytes. Biochem. Biophys. Res. Commun. 285: 926.931.
5. Nishikawa, K. C., and A. J. Millis. 2003. gp38k (CHI3L1) is a novel adhesion and migration factor for vascular cells. Exp. Cell Res. 287: 79.87.
6. Shackelton, L. M., D. M. Mann, and A. J. Millis. 1995. Identification of a 38-kDa heparin-binding glycoprotein (gp38k) in differentiating vascular smooth muscle cells as a member of a group of proteins associated with tissue remodeling. J. Biol. Chem. 270: 13076.13083.
7. Malinda, K. M., L. Ponce, H. K. Kleinman, L. M. Shackelton, and A. J. Millis. 1999. Gp38k, a protein synthesized by vascular smooth muscle cells, stimulates directional migration of human umbilical vein endothelial cells. Exp. Cell Res. 250: 168.173.
8. Singh, S. K., R. Bhardwaj, K. M. Wilczynska, C. I. Dumur, and T. Kordula. 2011. A complex of nuclear factor I-X3 and STAT3 regulates astrocyte and glioma migration through the secreted glycoprotein YKL-40. J. Biol. Chem. 286: 39893.39903.
9. Lee, C. G., D. Hartl, G. R. Lee, B. Koller, H. Matsuura, C. A. Da Silva, M. H. Sohn, L. Cohn, R. J. Homer, A. A. Kozhich, et al. 2009. Role of breast regression protein 39 (BRP-39)/chitinase 3-like-1 in Th2 and IL-13-induced tissue responses and apoptosis. J. Exp. Med. 206: 1149.1166.
10. Bonneh-Barkay, D., G. Wang, W. A. Laframboise, C. A. Wiley, and S. J. Bissel. 2012. Exacerbation of experimental autoimmune encephalomyelitis in the absence of breast regression protein 39/chitinase 3-like 1. J. Neuropathol. Exp. Neurol. 71: 948.958.
11. Sohn, M. H., M. J. Kang, H. Matsuura, V. Bhandari, N. Y. Chen, C. G. Lee, and J. A. Elias. 2010. The chitinase-like proteins breast regression protein-39 and YKL-40 regulate hyperoxia-induced acute lung injury. Am. J. Respir. Crit. Care Med. 182: 918.928.
12. Johansen, J. S., M. Stoltenberg, M. Hansen, A. Florescu, K. Harslev-Petersen, I. Lorenzen, and P. A. Price. 1999. Serum YKL-40 concentrations in patients with rheumatoid arthritis: relation to disease activity. Rheumatology 38: 618. 626.
13. Rathcke, C. N., J. S. Johansen, and H. Vestergaard. 2006. YKL-40, a biomarker of inflammation, is elevated in patients with type 2 diabetes and is related to insulin resistance. Inflamm. Res. 55: 53.59.
14. Rathcke, C. N., and H. Vestergaard. 2006. YKL-40, a new inflammatory marker with relation to insulin resistance and with a role in endothelial dysfunction and atherosclerosis. Inflamm. Res. 55: 221.227.
15. Hansen, M., A. R. Nielsen, T. Vilsball, A. Lund, T. Krarup, F. K. Knop, and H. Vestergaard. 2012. Increased levels of YKL-40 and interleukin 6 in patients with chronic pancreatitis and secondary diabetes. Pancreas 41: 1316.1318.
16. Konradsen, J. R., A. James, B. Nordlund, L. E. Reinius, C. Soderhall, E. Melen, A. M. Wheelock, K. C. Lodrup Carlsen, M. Lidegran, M. Verhoek, et al. 2013. The chitinase-like protein YKL-40: a possible biomarker of inflammation and airway remodeling in severe pediatric asthma. J. Allergy Clin. Immunol. 132: 328.335, e5.
17. Erzin, Y., H. Uzun, A. Karatas, and A. F. Celik. 2008. Serum YKL-40 as a marker of disease activity and stricture formation in patients with Crohns disease. J. Gastroenterol. Hepatol. 23: e357.e362.
18. Lee, S. H., C. Y. Lin, P. H. Wang, C. P. Han, S. F. Yang, J. T. Chang, M. C. Lee, L. Y. Lin, and M. S. Lee. 2012. Significant association of elevated concentration of plasma YKL-40 with disease severity in patients with pelvic inflammatory disease. J. Clin. Lab. Anal. 26: 136.142.
19. Johansen, J. S., S. Maller, P. A. Price, F. Bendtsen, J. Junge, C. Garbarsch, and J. H. Henriksen. 1997. Plasma YKL-40: a new potential marker of fibrosis in patients with alcoholic cirrhosis? Scand. J. Gastroenterol. 32: 582.590.
20. Craig-Schapiro, R., R. J. Perrin, C. M. Roe, C. Xiong, D. Carter, N. J. Cairns, M. A. Mintun, E. R. Peskind, G. Li, D. R. Galasko, et al. 2010. YKL-40: a novel prognostic fluid biomarker for preclinical Alzheimer's disease. Biol. Psychiatry 68: 903.912.
21. Bonneh-Barkay, D., S. J. Bissel, G. Wang, K. N. Fish, G. C. Nicholl, S. W. Darko, R. Medina-Flores, M. Murphey-Corb, P. A. Rajakumar, J. Nyaundi, et al. 2008. YKL-40, a marker of simian immunodeficiency virus encephalitis, modulates the biological activity of basic fibroblast growth factor. Am. J. Pathol. 173: 130.143.
22. Colton, C. A., R. T. Mott, H. Sharpe, Q. Xu, W. E. Van Nostrand, and M. P. Vitek. 2006. Expression profiles for macrophage alternative activation genes in AD and in mouse models of AD. J. Neuroinflammation 3: 27.
23. Comabella, M., M. Fernandez, R. Martin, S. Rivera-Vallve, E. Borras, C. Chiva, E. Julià, A. Rovira, E. Canto , J. C. Alvarez-Cermen.o, et al. 2010. Cerebrospinal fluid chitinase 3-like 1 levels are associated with conversion to multiple sclerosis. Brain 133: 1082.1093.
24. Kzhyshkowska, J., A. Gratchev, and S. Goerdt. 2007. Human chitinases and chitinase-like proteins as indicators for inflammation and cancer. Biomark. Insights 2: 128.146.
25. Ling, H., and A. D. Recklies. 2004. The chitinase 3-like protein human cartilage glycoprotein 39 inhibits cellular responses to the inflammatory cytokines interleukin-1 and tumour necrosis factor-a. Biochem. J. 380: 651.659.
26. Shao, R., K. Hamel, L. Petersen, Q. J. Cao, R. B. Arenas, C. Bigelow, B. Bentley, and W. Yan. 2009. YKL-40, a secreted glycoprotein, promotes tumor angiogenesis. Oncogene 28: 4456.4468.
27. Francescone, R. A., S. Scully, M. Faibish, S. L. Taylor, D. Oh, L. Moral, W. Yan, B. Bentley, and R. Shao. 2011. Role of YKL-40 in the angiogenesis, radioresistance, and progression of glioblastoma. J. Biol. Chem. 286: 15332.15343.
28. Recklies, A. D., H. Ling, C. White, and S. M. Bernier. 2005. Inflammatory cytokines induce production of CHI3L1 by articular chondrocytes. J. Biol. Chem. 280: 41213.41221.
29. Bonneh-Barkay, D., S. J. Bissel, J. Kofler, A. Starkey, G. Wang, and C. A. Wiley. 2012. Astrocyte and macrophage regulation of YKL-40 expression and cellular response in neuroinflammation. Brain Pathol. 22: 530.546.
30. Hayden, M. S., and S. Ghosh. 2008. Shared principles in NF-kB signaling. Cell 132: 344.362.
31. Pomerantz, J. L., and D. Baltimore. 2002. Two pathways to NF-kB. Mol. Cell 10: 693.695.
32. Oeckinghaus, A., M. S. Hayden, and S. Ghosh. 2011. Crosstalk in NF-kB signaling pathways. Nat. Immunol. 12: 695.708.
33. Derudder, E., E. Dejardin, L. L. Pritchard, D. R. Green, M. Korner, and V. Baud. 2003. RelB/p50 dimers are differentially regulated by tumor necrosis factor-a and lymphotoxin-b receptor activation: critical roles for p100. J. Biol. Chem. 278: 23278.23284.
34. Bhat, K. P., C. E. Pelloski, Y. Zhang, S. H. Kim, C. deLaCruz, M. Rehli, and K. D. Aldape. 2008. Selective repression of YKL-40 by NF-kB in glioma cell lines involves recruitment of histone deacetylase-1 and-2. FEBS Lett. 582: 3193.3200.
35. Bruce-Keller, A. J., J. Turchan-Cholewo, E. J. Smart, T. Geurin, A. Chauhan, R. Reid, R. Xu, A. Nath, P. E. Knapp, and K. F. Hauser. 2008. Morphine causes rapid increases in glial activation and neuronal injury in the striatum of inducible HIV-1 Tat transgenic mice. Glia 56: 1414.1427.
36. Stiene-Martin, A., R. Zhou, and K. F. Hauser. 1998. Regional, developmental, and cell cycle-dependent differences in m, d, and k-opioid receptor expression among cultured mouse astrocytes. Glia 22: 249.259.
37. Kordula, T., R. E. Rydel, E. F. Brigham, F. Horn, P. C. Heinrich, and J. Travis. 1998. Oncostatin M and the interleukin-6 and soluble interleukin-6 receptor complex regulate a1-antichymotrypsin expression in human cortical astrocytes. J. Biol. Chem. 273: 4112.4118.
38. Harikumar, K. B., J. W. Yester, M. J. Surace, C. Oyeniran, M. M. Price, W. C. Huang, N. C. Hait, J. C. Allegood, A. Yamada, X. Kong, et al. 2014. K63-linked polyubiquitination of transcription factor IRF1 is essential for IL-1.induced production of chemokines CXCL10 and CCL5. Nat. Immunol. 15: 231. 238.
39. Paugh, B. S., L. Bryan, S. W. Paugh, K. M. Wilczynska, S. M. Alvarez, S. K. Singh, D. Kapitonov, H. Rokita, S. Wright, I. Griswold-Prenner, et al. 2009. Interleukin-1 regulates the expression of sphingosine kinase 1 in glioblastoma cells. J. Biol. Chem. 284: 3408.3417.
40. Rehli, M., H. H. Niller, C. Ammon, S. Langmann, L. Schwarzfischer, R. Andreesen, and S. W. Krause. 2003. Transcriptional regulation of CHI3L1, a marker gene for late stages of macrophage differentiation. J. Biol. Chem. 278: 44058.44067.
41. Leon, L. R., C. A. Conn, M. Glaccum, and M. J. Kluger. 1996. IL-1 type I receptor mediates acute phase response to turpentine, but not lipopolysaccharide, in mice. Am. J. Physiol. 271: R1668.R1675.
42. Glibetic, M. D., and H. Baumann. 1986. Influence of chronic inflammation on the level of mRNA for acute-phase reactants in the mouse liver. J. Immunol. 137: 1616.1622.
43. Kothavale, A., D. Di Gregorio, F. P. Somera, and M. E. Smith. 1995. GFAP mRNA fluctuates in synchrony with chronic relapsing EAE symptoms in SJL/J mice. Glia 14: 216.224.
44. Lee, W. H., W. E. Sonntag, M. Mitschelen, H. Yan, and Y. W. Lee. 2010. Irradiation induces regionally specific alterations in pro-inflammatory environments in rat brain. Int. J. Radiat. Biol. 86: 132.144.
45. Fitting, S., S. Zou,W. Chen, P. Vo, K. F. Hauser, and P. E. Knapp. 2010. Regional heterogeneity and diversity in cytokine and chemokine production by astroglia: differential responses to HIV-1 Tat, gp120, and morphine revealed by multiplex analysis. J. Proteome Res. 9: 1795.1804.
46. Liberto, C. M., P. J. Albrecht, L. M. Herx, V. W. Yong, and S. W. Levison. 2004. Pro-regenerative properties of cytokine-activated astrocytes. J. Neurochem. 89: 1092.1100.
47. Heinrich, P. C., I. Behrmann, G. Müller-Newen, F. Schaper, and L. Graeve. 1998. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 334: 297.314.
48. Letuve, S., A. Kozhich, N. Arouche, M. Grandsaigne, J. Reed, M. C. Dombret, P. A. Kiener, M. Aubier, A. J. Coyle, and M. Pretolani. 2008. YKL-40 is elevated in patients with chronic obstructive pulmonary disease and activates alveolar macrophages. J. Immunol. 181: 5167.5173.
49. Kuepper, M., K. Bratke, and J. C. Virchow. 2008. Chitinase-like protein and asthma. N. Engl. J. Med. 358: 1073.1075, author reply 1075.
50. Johansen, J. S. 2006. Studies on serum YKL-40 as a biomarker in diseases with inflammation, tissue remodelling, fibroses and cancer. Dan. Med. Bull. 53: 172.209.
51. Gross, O., C. J. Thomas, G. Guarda, and J. Tschopp. 2011. The inflammasome: an integrated view. Immunol. Rev. 243: 136.151.
52. Norris, J. G., L. P. Tang, S. M. Sparacio, and E. N. Benveniste. 1994. Signal transduction pathways mediating astrocyte IL-6 induction by IL-1b and tumor necrosis factor-a. J. Immunol. 152: 841.850.
53. Sparacio, S. M., Y. Zhang, J. Vilcek, and E. N. Benveniste. 1992. Cytokine regulation of interleukin-6 gene expression in astrocytes involves activation of an NF-kB.like nuclear protein. J. Neuroimmunol. 39: 231.242.
54. Bode, J. G., U. Albrecht, D. Haussinger, P. C. Heinrich, and F. Schaper. 2012. Hepatic acute phase proteins.regulation by IL-6-and IL-1-type cytokines involving STAT3 and its crosstalk with NF-kB.dependent signaling. Eur. J. Cell Biol. 91: 496.505.
55. He, C. H., C. G. Lee, C. S. Dela Cruz, C. M. Lee, Y. Zhou, F. Ahangari, B. Ma, E. L. Herzog, S. A. Rosenberg, Y. Li, et al. 2013. Chitinase 3-like 1 regulates cellular and tissue responses via IL-13 receptor a2. Cell Reports 4: 830.841.
56. Bara, I., A. Ozier, P. O. Girodet, G. Carvalho, J. Cattiaux, H. Begueret, M. Thumerel, O. Ousova, R. Kolbeck, A. J. Coyle, et al. 2012. Role of YKL-40 in bronchial smooth muscle remodeling in asthma. Am. J. Respir. Crit. Care Med. 185: 715.722.
57. Rallabhandi, P., Q. M. Nhu, V. Y. Toshchakov, W. Piao, A. E. Medvedev, M. D. Hollenberg, A. Fasano, and S. N. Vogel. 2008. Analysis of proteinaseactivated receptor 2 and TLR4 signal transduction: a novel paradigm for receptor cooperativity. J. Biol. Chem. 283: 24314.24325.
58. Matsusaka, T., K. Fujikawa, Y. Nishio, N. Mukaida, K. Matsushima, T. Kishimoto, and S. Akira. 1993. Transcription factors NF-IL6 and NF-kB synergistically activate transcription of the inflammatory cytokines, interleukin 6 and interleukin 8. Proc. Natl. Acad. Sci. USA 90: 10193.10197.
59. Bonizzi, G., and M. Karin. 2004. The two NF-kB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25: 280.288.
60. Shih, V. F., J. Davis-Turak, M. Macal, J. Q. Huang, J. Ponomarenko, J. D. Kearns, T. Yu, R. Fagerlund, M. Asagiri, E. I. Zuniga, and A. Hoffmann. 2012. Control of RelB during dendritic cell activation integrates canonical and noncanonical NF-kB pathways. Nat. Immunol. 13: 1162.1170.
61. Kobayashi, T., P. T.Walsh, M. C. Walsh, K. M. Speirs, E. Chiffoleau, C. G. King, W. W. Hancock, J. H. Caamano, C. A. Hunter, P. Scott, et al. 2003. TRAF6 is a critical factor for dendritic cell maturation and development. Immunity 19: 353.363.
62. Sun, S. C. 2012. The noncanonical NF-kB pathway. Immunol. Rev. 246: 125. 140.
63. Bhat, K. P., V. Balasubramaniyan, B. Vaillant, R. Ezhilarasan, K. Hummelink, F. Hollingsworth, K. Wani, L. Heathcock, J. D. James, L. D. Goodman, et al. 2013. Mesenchymal differentiation mediated by NF-kB promotes radiation resistance in glioblastoma. Cancer Cell 24: 331.346.
64. Lee, D. W., D. Ramakrishnan, J. Valenta, I. F. Parney, K. J. Bayless, and R. Sitcheran. 2013. The NF-kB RelB protein is an oncogenic driver of mesenchymal glioma. PLoS One 8: e57489.