Osteopontin enhances the migration of lung fibroblasts via upregulation of interleukin-6 through the extracellular signal-regulated kinase (ERK) pathway

References

Agnihotri, R., Crawford, H.C., Haro, H., Matrisian, L.M., Havrda, M.C., and Liaw, L. (2001). Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin). J. Biol. Chem. 276: 28261–28267, https://doi.org/10.1074/jbc.m103608200.10.1074/jbc.M103608200Search in Google Scholar PubMed

Ahluwalia, N., Shea, B.S., and Tager, A.M. (2014). New therapeutic targets in idiopathic pulmonary fibrosis. Aiming to rein in runaway wound-healing responses. Am. J. Respir. Crit. Care. Med. 190: 867–878, https://doi.org/10.1164/rccm.201403-0509PP.10.1164/rccm.201403-0509PPSearch in Google Scholar PubMed PubMed Central

Ataie-Kachoie, P., Pourgholami, M.H., Richardson, D.R., and Morris, D.L. (2014). Gene of the month: interleukin 6 (IL-6). J. Clin. Pathol. 67: 932–937, https://doi.org/10.1136/jclinpath-2014-202493.10.1136/jclinpath-2014-202493Search in Google Scholar PubMed

Aumiller, V., Balsara, N., Wilhelm, J., Günther, A., and Königshoff, M. (2013). WNT/β-catenin signaling induces IL-1β expression by alveolar epithelial cells in pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 49: 96–104, https://doi.org/10.1165/rcmb.2012-0524OC.10.1165/rcmb.2012-0524OCSearch in Google Scholar PubMed

Castello, L.M., Raineri, D., Salmi, L., Clemente, N., Vaschetto, R., Quaglia, M., Garzaro, M., Gentilli, S., and Navalesi, P., Cantaluppi, V. (2017). Osteopontin at the crossroads of inflammation and tumor progression. Mediat. Inflamm. 2017: 4049098, https://doi.org/10.1155/2017/4049098.10.1155/2017/4049098Search in Google Scholar PubMed PubMed Central

Fielding, C.A., Jones, G.W., McLoughlin, R.M., McLeod, L., Hammond, V.J., Uceda, J., Williams, A.S., Lambie, M., Foster, T.L., Liao, C.T.Rice, C.M., Greenhill, C.J., Colmont, C.S., Hams, E., Coles, B., Kift Morgan, A., Newton, Z., Craig, K.J., Williams, J.D. Williams, G.T. Davies, S.J. Humphreys, I.R. O’Donnell, V.B.Taylor, P.R. Jenkins, B.J. Topley, N. Jones, S.A. (2014). Interleukin-6 signaling drives fibrosis in unresolved inflammation. Immunity 40: 40–50, https://doi.org/10.1016/j.immuni.2013.10.022.10.1016/j.immuni.2013.10.022Search in Google Scholar PubMed PubMed Central

Gallucci, R.M., Sloan, D.K., Heck, J.M., Murray, A.R., and O’Dell, S.J. (2004). Interleukin 6 indirectly induces keratinocyte migration. J. Invest. Dermatol. 122: 764–772, https://doi.org/10.1111/j.0022-202X.2004.22323.x.10.1111/j.0022-202X.2004.22323.xSearch in Google Scholar PubMed

Gasse, P., Mary, C., Guenon, I., Noulin, N., Charron, S., Schnyder-candrian, S., Schnyder, B., Akira, S., and Quesniaux, V.F.J., Lagente, V., Ryffel, B., Couillin, I. (2007). IL-1R1 / MyD88 signaling and the inflammasome are essential in pulmonary inflammation and fibrosis in mice. J. Clin. Invest. 117, 3786–3799, https://doi.org/10.1172/JCI32285.10.1172/JCI32285Search in Google Scholar PubMed PubMed Central

Hoshino, T., Okamoto, M., Sakazaki, Y., Kato, S., Young, H.A., and Aizawa, H. (2009). Role of proinflammatory cytokines IL-18 and IL-1β in bleomycin-induced lung injury in humans and mice. Am. J. Respir. Cell Mol. Biol. 41: 661–670, https://doi.org/10.1165/rcmb.2008-0182OC.10.1165/rcmb.2008-0182OCSearch in Google Scholar PubMed

Kuhn, C., Boldt, J., King, T.E.Jr., Crouch, E., Vartio, T., and McDonald, J.A. (1989). An immunohistochemical study of architectural remodeling and connective tissue synthesis in pulmonary fibrosis. Am. Rev. Respir. Dis. 140: 1693–1703, https://doi.org/10.1164/ajrccm/140.6.1693.10.1164/ajrccm/140.6.1693Search in Google Scholar PubMed

Kulkarni, T., O’Reilly, P., Antony, V.B., Gaggar, A., and Thannickal, V.J. (2016). Matrix remodeling in pulmonary fibrosis and emphysema. Am. J. Respir. Cell Mol. Biol. 54: 751–760, https://doi.org/10.1165/rcmb.2015-0166PS.10.1165/rcmb.2015-0166PSSearch in Google Scholar PubMed PubMed Central

Lee, G.L., Wu, J.Y., Tsai, C.S., Lin, C.Y., Tsai, Y.T., Lin, C.S., Wang, Y.F., Yet, S.F., Hsu, Y.J., and Kuo, C.C. (2016). TLR4-activated MAPK-IL-6 axis regulates vascular smooth muscle cell function. Int. J. Mol. Sci. 17: 1394, https://doi.org/10.3390/ijms17091394.10.3390/ijms17091394Search in Google Scholar PubMed PubMed Central

Liang, C.C., Park, A.Y., and Guan, J.L. (2007). In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat. Protoc. 2: 329–333, https://doi.org/10.1038/nprot.2007.30.10.1038/nprot.2007.30Search in Google Scholar PubMed

Liang, J., Xu, L., Zhou, F., Liu, A.M., Ge, H.X., Chen, Y.Y., and Tu, M. (2018). MALAT1/miR-127-5p regulates osteopontin (OPN)-mediated proliferation of human chondrocytes through PI3K/Akt pathway. J Cell Biochem. 119: 431–439, https://doi.org/10.1002/jcb.26200.10.1002/jcb.26200Search in Google Scholar PubMed

Ma, F., Li, Y., Jia, L., Han, Y., Cheng, J., Li, H., Qi, Y., and Du, J. (2012). Macrophage-stimulated cardiac fibroblast production of IL-6 is essential for TGF β/smad activation and cardiac fibrosis induced by angiotensin II. PLoS One 7: 1–9, https://doi.org/10.1371/journal.pone.0035144.10.1371/journal.pone.0035144Search in Google Scholar PubMed PubMed Central

Many, G.M., Yokosaki, Y., Uaesoontrachoon, K., Nghiem, P.P., Bello, L., Dadgar, S., Yin, Y., Damsker, J.M., Cohen, H.B., Kornegay, J.N., Bamman, M.M., Mosser, D.M., Nagaraju, K., Hoffman, E.P. (2016). OPN-a induces muscle inflammation by increasing recruitment and activation of pro-inflammatory macrophages. Exp. Physiol. 101: 1285–1300, https://doi.org/10.1113/EP085768.10.1113/EP085768Search in Google Scholar PubMed PubMed Central

Meléndez, G.C. and Hundley, W.G. (2016). Is myocardial fibrosis a new Frontier for discovery in cardiotoxicity related to the administration of anthracyclines?. Circ. Cardiovasc. Imag. 9: e005797, https://doi.org/10.1161/circimaging.116.005797.10.1161/CIRCIMAGING.116.005797Search in Google Scholar PubMed PubMed Central

Meléndez, G.C., McLarty, J.L., Levick, S.P., Du, Y., Janicki, J.S., and Brower, G.L. (2010). Interleukin 6 mediates myocardial fibrosis, concentric hypertrophy, and diastolic dysfunction in rats. Hypertension 56: 225–231, https://doi.org/10.1161/HYPERTENSIONAHA.109.148635.10.1161/HYPERTENSIONAHA.109.148635Search in Google Scholar PubMed PubMed Central

Nau, G.J., Guilfoile, P., Chupp, G.L., Berman, J.S., Kim, S.J., Kornfeld, H., and Young, R.A. (1997). A chemoattractant cytokine associated with granulomas in tuberculosis and silicosis. Proc. Natl. Acad. Sci. USA 94: 6414–6419, https://doi.org/10.1073/pnas.94.12.6414.10.1073/pnas.94.12.6414Search in Google Scholar PubMed PubMed Central

Nonaka, K., Kajiura, Y., Bando, M., Sakamoto, E., Inagaki, Y., Lew, J.H., Naruishi, K., Ikuta, T., Yoshida, K., Kobayashi, T., Yoshie, H., Nagata, T., Kido, J. (2018). Advanced glycation end-products increase IL-6 and ICAM-1 expression via RAGE, MAPK and NF-κB pathways in human gingival fibroblasts. J. Periodontal. Res. 53: 334–344, https://doi.org/10.1111/jre.12518.10.1111/jre.12518Search in Google Scholar PubMed

O’Regan, A.W., Chupp, G.L., Lowry, J.A., Goetschkes, M., Mulligan, N., and Berman, J.S. (1999). Osteopontin is associated with T cells in sarcoid granulomas and has T cell adhesive and cytokine-like properties in vitro. J. Immunol. 162: 1024–1031.10.4049/jimmunol.162.2.1024Search in Google Scholar

Pan, L.H., Ohtani, H., Yamauchi, K., and Nagura, H. (1996). Co-expression of TNFα and IL-1β in human acute pulmonary fibrotic diseases: an immunohistochemical analysis. Pathol. Int. 46: 91–99, https://doi.org/10.1111/j.1440-1827.1996.tb03584.x.10.1111/j.1440-1827.1996.tb03584.xSearch in Google Scholar PubMed

Pardo, A., Gibson, K., Cisneros, J., Richards, T.J., Yang, Y., Becerril, C., Yousem, S., Herrera, I., and Ruiz, V., Selman, M., and Kaminski, N. (2005). Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med. 2: 0891–0903, https://doi.org/10.1371/journal.pmed.0020251.10.1371/journal.pmed.0020251Search in Google Scholar PubMed PubMed Central

Pazolli, E., Luo, X., Brehm, S., Carbery, K., Chung, J.J., Prior, J.L., Doherty, J., Demehri, S., and Salavaggione, L., Piwnica-Worms, D., Stewart, S.A. (2009). Senescent stromal-derived osteopontin promotes preneoplastic cell growth. Cancer Res. 69: 1230–1239, https://doi.org/10.1158/0008-5472.CAN-08-2970.10.1158/0008-5472.CAN-08-2970Search in Google Scholar PubMed PubMed Central

Prasse, A., Pechkovsky, D.V., Toews, G.B., Jungraithmayr, W., Kollert, F., Goldmann, T., Vollmer, E., Müller-Quernheim, J., and Zissel, G. (2006). A vicious circle of alveolar macrophages and fibroblasts perpetuates pulmonary fibrosis via CCL18. Am. J. Respir. Crit. Care Med. 173: 781–792, https://doi.org/10.1164/rccm.200509-1518OC.10.1164/rccm.200509-1518OCSearch in Google Scholar PubMed

Ray, S., Ju, X., Sun, H., Finnerty, C.C., Herndon, D.N., and Brasier, A.R. (2013). The IL-6 trans-signaling-STAT3 pathway mediates ECM and cellular proliferation in fibroblasts from hypertrophic scar. J. Invest. Dermatol. 133: 1212–1220, https://doi.org/10.1038/jid.2012.499.10.1038/jid.2012.499Search in Google Scholar PubMed PubMed Central

Samuvel, D.J., Sundararaj, K.P., Li, Y., Lopes-Virella, M.F., and Huang, Y. (2010). Adipocyte-mononuclear cell interaction, Toll-like receptor 4 activation, and high glucose synergistically up-regulate osteopontin expression via an interleukin 6-mediated mechanism. J. Biol. Chem. 285: 3916–3927, https://doi.org/10.1074/jbc.m109.033951.10.1074/jbc.M109.033951Search in Google Scholar PubMed PubMed Central

Shen, T.N., Kanazawa, S., Kado, M., Okada, K., Luo, L., Hayashi, A., Mizuno, H., and Tanaka, R. (2017). Interleukin-6 stimulates Akt and p38 MAPK phosphorylation and fibroblast migration in non-diabetic but not diabetic mice. PLoS One 12: e0178232, https://doi.org/10.1371/journal.pone.0178232.10.1371/journal.pone.0178232Search in Google Scholar PubMed PubMed Central

Shimodaira, T., Matsuda, K., Uchibori, T., Sugano, M., Uehara, T., and Honda, T. (2018). Upregulation of osteopontin expression via the interaction of macrophages and fibroblasts under IL-1b stimulation. Cytokine 110: 63–69, https://doi.org/10.1016/j.cyto.2018.04.025.10.1016/j.cyto.2018.04.025Search in Google Scholar PubMed

Suganuma, H., Sato, A., Tamura, R., and Chida, K. (1995). Enhanced migration of fibroblasts derived from lungs with fibrotic lesions. Thorax 50: 984–989, https://doi.org/10.1136/thx.50.9.984.10.1136/thx.50.9.984Search in Google Scholar PubMed PubMed Central

Tager, A.M., LaCamera, P., Shea, B.S., Campanella, G.S., Selman, M., Zhao, Z., Polosukhin, V., Wain, J., and Karimi-Shah, B.A., Kim, N.D., Hart, W.K., Pardo, A., Blackwell, T.S., Xu, Y., Chun, J., Luster, A.D. (2008). The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nat. Med. 14: 45–54, https://doi.org/10.1038/nm1685.10.1038/nm1685Search in Google Scholar PubMed

Take, Y., Nakata, K., Hashimoto, J., Tsuboi, H., Nishimoto, N., Ochi, T., and Yoshikawa, H. (2009). Specifically modified osteopontin in rheumatoid arthritis fibroblast-like synoviocytes supports interaction with B cells and enhances production of interleukin-6. Arthritis Rheum. 60: 3591–3601, https://doi.org/10.1002/art.25020.10.1002/art.25020Search in Google Scholar PubMed

Tsukui, T., Ueha, S., Abe, J., Hashimoto, S., Shichino, S., Shimaoka, T., Shand, F.H., Arakawa, Y., Oshima, K., Hattori, M., Inagaki, Y., Tomura, M., Matsushima, K. (2013). Qualitative rather than quantitative changes are hallmarks of fibroblasts in bleomycin-induced pulmonary fibrosis. Am. J. Pathol. 183: 758–773, https://doi.org/10.1016/j.ajpath.2013.06.005.10.1016/j.ajpath.2013.06.005Search in Google Scholar PubMed

Tsukui, T., Ueha, S., Shichino, S., Inagaki, Y., and Matsushima, K. (2015). Intratracheal cell transfer demonstrates the profibrotic potential of resident fibroblasts in pulmonary fibrosis. Am. J. Pathol. 185: 2939–2948, https://doi.org/10.1016/j.ajpath.2015.07.022.10.1016/j.ajpath.2015.07.022Search in Google Scholar PubMed

Tsukui, T., Ueha, S., Shichino, S., Hashimoto, S., Nakajima, T., Shiraishi, K., Kihara, M., Kiyonari, H., Inagaki, Y., and Matsushima, K. (2019). Gli signaling pathway modulates fibroblast activation and facilitates scar formation in pulmonary fibrosis. Biochem. Biophys. Res. Commun. 514: 684–690, https://doi.org/10.1016/j.bbrc.2019.05.011.10.1016/j.bbrc.2019.05.011Search in Google Scholar PubMed

Wang, K.X. and Denhardt, D.T. (2008). Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev. 19: 333–345, https://doi.org/10.1016/j.cytogfr.2008.08.001.10.1016/j.cytogfr.2008.08.001Search in Google Scholar PubMed

Wei, L., Xiong, H., Li, W., Li, B., and Cheng, Y. (2018). Upregulation of IL-6 expression in human salivary gland cell line by IL-17 via activation of p38 MAPK, ERK, PI3K/Akt, and NF-κB pathways. J. Oral. Pathol. Med. 47: 847–855, https://doi.org/10.1111/jop.12765.10.1111/jop.12765Search in Google Scholar PubMed

Wilson, M.S. and Wynn, T.A. (2009). Pulmonary fibrosis: Pathogenesis, etiology and regulation. Mucosal. Immunol. 2: 103–121, https://doi.org/10.1038/mi.2008.85.10.1038/mi.2008.85Search in Google Scholar PubMed PubMed Central

Wilson, M.S., Madala, S.K., Ramalingam, T.R., Gochuico, B.R., Rosas, I.O., Cheever, A.W., and Wynn, T.A. (2010). Bleomycin and IL-1β–mediated pulmonary fibrosis is IL- 17A dependent. J. Exp. Med. 207: 535–552, https://doi.org/10.1084/jem.20092121.10.1084/jem.20092121Search in Google Scholar PubMed PubMed Central

Wu, X., Tao, P., Zhou, Q., Li, J., Yu, Z., Wang, X., Li, J., Li, C., and Yan, M., Zhu, Z., Liu, B., Su, L. (2017). IL-6 secreted by cancer-associated fibroblasts promotes epithelial-mesenchymal transition and metastasis of gastric cancer via JAK2/STAT3 signaling pathway. Oncotarget 8: 20741–20750, https://doi.org/10.18632/oncotarget.15119.10.18632/oncotarget.15119Search in Google Scholar PubMed PubMed Central

Xu, J., Yi, Y., Li, L., Zhang, W., and Wang, J. (2015). Osteopontin induces vascular endothelial growth factor expression in articular cartilage through PI3K/AKT and ERK1/2 signaling. Mol. Med. Rep. 12: 4708–4712, https://doi.org/10.3892/mmr.2015.3975.10.3892/mmr.2015.3975Search in Google Scholar PubMed

Yang, Y., Gao, S.G., Zhang, F.J., Luo, W., Xue, J.X., and Lei, G.H. (2014). Effects of osteopontin on the expression of IL-6 and IL-8 inflammatory factors in human knee osteoarthritis chondrocytes. Eur. Rev. Med. Pharmacol. Sci. 18: 3580–3586.Search in Google Scholar

Yang, M., Wang, X., Wang, L., Wang, X., Li, J., and Yang, Z. (2017). IL-1α up-regulates IL-6 expression in bovine granulosa cells via MAPKs and NF-κB signaling pathways. Cell. Physiol. Biochem. 41: 265–273, https://doi.org/10.1159/000456091.10.1159/000456091Search in Google Scholar PubMed

Yoshida, K., Kuwano, K., Hagimoto, N., Watanabe, K., Matsuba, T., Fujita, M., Inoshima, I., and Hara, N. (2002). MAP kinase activation and apoptosis in lung tissues from patients with idiopathic pulmonary fibrosis. J. Pathol. 198: 388–396, 10.1002/path.1208.10.1002/path.1208Search in Google Scholar PubMed

Zou, C., Luo, Q., Qin, J., Shi, Y., Yang, L., Ju, B., and Song, G. (2013). Osteopontin promotes mesenchymal stem cell migration and lessens cell stiffness via integrin β1, FAK, and ERK pathways. Cell. Biochem. Biophys. 65: 455–462, https://doi.org/10.1007/s12013-012-9449-8.10.1007/s12013-012-9449-8Search in Google Scholar PubMed

Zuo, F., Kaminski, N., Eugui, E., Allard, J., Yakhini, Z., Ben-Dor, A., Lollini, L., Morris, D., Kim, Y., DeLustro, B., Sheppard, D., Pardo, A., Selman, M., Heller, R.A. (2002). Gene expression analysis reveals matrilysin as a key regulator of pulmonary fibrosis in mice and humans. Proc. Natl. Acad. Sci. USA 99: 6292–6297, https://doi.org/10.1073/pnas.092134099.10.1073/pnas.092134099Search in Google Scholar PubMed PubMed Central