Skip to main content
Top
Published in: Inflammation 1/2020

01-02-2020 | Arthritis | Original Article

Changes in Radixin Expression and Interaction with Efflux Transporters in the Liver of Adjuvant-Induced Arthritic Rats

Authors: Atsushi Kawase, Misaki Nakasaka, Hatsune Bando, Saori Yasuda, Hiroaki Shimada, Masahiro Iwaki

Published in: Inflammation | Issue 1/2020

Login to get access

Abstract

Scaffold proteins such as radixin help to modulate the plasma membrane localization and transport activity of the multidrug resistance-associated protein 2 (MRP2/ABCC2) and P-glycoprotein (P-gp/ABCB1) efflux transporters in the liver. We examined changes in radixin expression and interaction with efflux transporters in adjuvant-induced arthritic (AA) rats, an animal model of rheumatoid arthritis, as well as in human liver cancer (HepG2) cells because inflammation affects drug pharmacokinetics via the efflux transporters. The expression levels of radixin and phosphorylated radixin (p-radixin) were measured 24 h after treatment with inflammatory cytokines comprising tumor necrosis factor (TNF)-α, interleukin (IL)-1β, IL-6 or sodium nitroprusside (SNP; a nitric oxide donor). The protein levels of radixin, MRP2, and P-gp in the rat liver were next examined. We also investigated whether inflammation affected the formation of complexes between radixin and MRP2 or P-gp. The mRNA and protein levels of radixin in HepG2 cells were significantly decreased by TNF-α treatment, while minimal changes were observed after treatment with IL-1β, IL-6 or SNP. TNF-α also significantly decreased the protein levels of p-radixin, suggesting that TNF-α inhibited the activation of radixin and thereby reduced the activity of the efflux transporters. Complex formation of radixin with MRP2 and P-gp was significantly decreased in AA rats but this was reversed by prednisolone and dexamethasone treatment, indicating that decreased interactions of radixin with MRP2 and P-gp likely occur during liver inflammation. These data suggest that liver inflammation reduces radixin function by decreasing its interactions with MRP2 and P-gp.
Literature
1.
go back to reference Stieger, B., K. Fattinger, J. Madon, G.A. Kullak-Ublick, and P.J. Meier. 2000. Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver. Gastroenterology 118: 422–430.CrossRef Stieger, B., K. Fattinger, J. Madon, G.A. Kullak-Ublick, and P.J. Meier. 2000. Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver. Gastroenterology 118: 422–430.CrossRef
2.
go back to reference Sato, N., N. Funayama, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1992. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. Journal of Cell Science 103 ( Pt 1: 131–143.PubMed Sato, N., N. Funayama, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita. 1992. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. Journal of Cell Science 103 ( Pt 1: 131–143.PubMed
3.
go back to reference Kojima, Hideyuki, Anne T. Nies, Jörg König, Wolfgang Hagmann, Herbert Spring, Masahito Uemura, Hiroshi Fukui, and Dietrich Keppler. 2003. Changes in the expression and localization of hepatocellular transporters and radixin in primary biliary cirrhosis. Journal of Hepatology 39: 693–702.CrossRef Kojima, Hideyuki, Anne T. Nies, Jörg König, Wolfgang Hagmann, Herbert Spring, Masahito Uemura, Hiroshi Fukui, and Dietrich Keppler. 2003. Changes in the expression and localization of hepatocellular transporters and radixin in primary biliary cirrhosis. Journal of Hepatology 39: 693–702.CrossRef
7.
go back to reference Yonemura, Shigenobu, Takeshi Matsui, Shoichiro Tsukita, and Sachiko Tsukita. 2002. Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: An essential role for polyphosphoinositides in vivo. Journal of Cell Science 115: 2569–2580.PubMed Yonemura, Shigenobu, Takeshi Matsui, Shoichiro Tsukita, and Sachiko Tsukita. 2002. Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: An essential role for polyphosphoinositides in vivo. Journal of Cell Science 115: 2569–2580.PubMed
8.
go back to reference Pietromonaco, S.F., P.C. Simons, A. Altman, and L. Elias. 1998. Protein kinase C-theta phosphorylation of moesin in the actin-binding sequence. The Journal of Biological Chemistry 273: 7594–7603.CrossRef Pietromonaco, S.F., P.C. Simons, A. Altman, and L. Elias. 1998. Protein kinase C-theta phosphorylation of moesin in the actin-binding sequence. The Journal of Biological Chemistry 273: 7594–7603.CrossRef
9.
go back to reference Kikuchi, Shojiro, Masaki Hata, Kanehisa Fukumoto, Yukari Yamane, Takeshi Matsui, Atsushi Tamura, Shigenobu Yonemura, Hisakazu Yamagishi, Dietrich Keppler, Shoichiro Tsukita, and Sachiko Tsukita. 2002. Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nature Genetics 31: 320–325. https://doi.org/10.1038/ng905.CrossRefPubMed Kikuchi, Shojiro, Masaki Hata, Kanehisa Fukumoto, Yukari Yamane, Takeshi Matsui, Atsushi Tamura, Shigenobu Yonemura, Hisakazu Yamagishi, Dietrich Keppler, Shoichiro Tsukita, and Sachiko Tsukita. 2002. Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nature Genetics 31: 320–325. https://​doi.​org/​10.​1038/​ng905.CrossRefPubMed
12.
go back to reference Belpaire, F.M., F. de Smet, B. Chindavijak, N. Fraeyman, and M.G. Bogaert. 1989. Effect of turpentine-induced inflammation on the disposition kinetics of propranolol, metoprolol, and antipyrine in the rat. Fundamental & Clinical Pharmacology 3: 79–88.CrossRef Belpaire, F.M., F. de Smet, B. Chindavijak, N. Fraeyman, and M.G. Bogaert. 1989. Effect of turpentine-induced inflammation on the disposition kinetics of propranolol, metoprolol, and antipyrine in the rat. Fundamental & Clinical Pharmacology 3: 79–88.CrossRef
13.
go back to reference Piquette-Miller, M., and F. Jamali. 1993. Selective effect of adjuvant arthritis on the disposition of propranolol enantiomers in rats detected using a stereospecific HPLC assay. Pharmaceutical Research 10: 294–299.CrossRef Piquette-Miller, M., and F. Jamali. 1993. Selective effect of adjuvant arthritis on the disposition of propranolol enantiomers in rats detected using a stereospecific HPLC assay. Pharmaceutical Research 10: 294–299.CrossRef
15.
go back to reference Piquette-Miller, M., and F. Jamali. 1992. Effect of adjuvant arthritis on the disposition of acebutolol enantiomers in rats. Agents and Actions 37: 290–296.CrossRef Piquette-Miller, M., and F. Jamali. 1992. Effect of adjuvant arthritis on the disposition of acebutolol enantiomers in rats. Agents and Actions 37: 290–296.CrossRef
16.
go back to reference Schneider, R.E., H. Bishop, M.J. Kendall, and C.P. Quarterman. 1981. Effect of inflammatory disease on plasma concentrations of three beta-adrenoceptor blocking agents. International Journal of Clinical Pharmacology, Therapy, and Toxicology 19: 158–162.PubMed Schneider, R.E., H. Bishop, M.J. Kendall, and C.P. Quarterman. 1981. Effect of inflammatory disease on plasma concentrations of three beta-adrenoceptor blocking agents. International Journal of Clinical Pharmacology, Therapy, and Toxicology 19: 158–162.PubMed
18.
go back to reference Kawase, Atsushi, Sari Norikane, Ayaka Okada, Mamiko Adachi, Yukio Kato, and Masahiro Iwaki. 2014. Distinct alterations in ATP-binding cassette transporter expression in liver, kidney, small intestine, and brain in adjuvant-induced arthritic rats. Journal of Pharmaceutical Sciences 103: 2556–2564. https://doi.org/10.1002/jps.24043.CrossRefPubMed Kawase, Atsushi, Sari Norikane, Ayaka Okada, Mamiko Adachi, Yukio Kato, and Masahiro Iwaki. 2014. Distinct alterations in ATP-binding cassette transporter expression in liver, kidney, small intestine, and brain in adjuvant-induced arthritic rats. Journal of Pharmaceutical Sciences 103: 2556–2564. https://​doi.​org/​10.​1002/​jps.​24043.CrossRefPubMed
20.
go back to reference Williams, R.C. 1992. Rheumatoid factors: Historical perspective, origins and possible role in disease. The Journal of Rheumatology. Supplement 32: 42–45.PubMed Williams, R.C. 1992. Rheumatoid factors: Historical perspective, origins and possible role in disease. The Journal of Rheumatology. Supplement 32: 42–45.PubMed
22.
go back to reference Kawase, Atsushi, Misato Sakata, Nagisa Yada, Misaki Nakasaka, Takuya Shimizu, Yukio Kato, and Masahiro Iwaki. 2014. Decreased radixin function for ATP-binding cassette transporters in liver in adjuvant-induced arthritis rats. Journal of Pharmaceutical Sciences 103: 4058–4065. https://doi.org/10.1002/jps.24210.CrossRefPubMed Kawase, Atsushi, Misato Sakata, Nagisa Yada, Misaki Nakasaka, Takuya Shimizu, Yukio Kato, and Masahiro Iwaki. 2014. Decreased radixin function for ATP-binding cassette transporters in liver in adjuvant-induced arthritis rats. Journal of Pharmaceutical Sciences 103: 4058–4065. https://​doi.​org/​10.​1002/​jps.​24210.CrossRefPubMed
23.
go back to reference Kawase, Atsushi, Akiyuki Fujii, Makiko Negoro, Ryosuke Akai, Miki Ishikubo, Hiroshi Komura, and Masahiro Iwaki. 2008. Differences in cytochrome P450 and nuclear receptor mRNA levels in liver and small intestines between SD and DA rats. Drug Metabolism and Pharmacokinetics 23: 196–206.CrossRef Kawase, Atsushi, Akiyuki Fujii, Makiko Negoro, Ryosuke Akai, Miki Ishikubo, Hiroshi Komura, and Masahiro Iwaki. 2008. Differences in cytochrome P450 and nuclear receptor mRNA levels in liver and small intestines between SD and DA rats. Drug Metabolism and Pharmacokinetics 23: 196–206.CrossRef
24.
go back to reference Kawase, Atsushi, Ayano Yamada, Yuko Gamou, Chika Tahara, Fumiaki Takeshita, Kazuya Murata, Hideaki Matsuda, Keiichi Samukawa, and Masahiro Iwaki. 2013. Increased effects of ginsenosides on the expression of cholesterol 7α-hydroxylase but not the bile salt export pump are involved in cholesterol metabolism. Journal of Natural Medicines 67: 545–553. https://doi.org/10.1007/s11418-012-0713-4.CrossRefPubMed Kawase, Atsushi, Ayano Yamada, Yuko Gamou, Chika Tahara, Fumiaki Takeshita, Kazuya Murata, Hideaki Matsuda, Keiichi Samukawa, and Masahiro Iwaki. 2013. Increased effects of ginsenosides on the expression of cholesterol 7α-hydroxylase but not the bile salt export pump are involved in cholesterol metabolism. Journal of Natural Medicines 67: 545–553. https://​doi.​org/​10.​1007/​s11418-012-0713-4.CrossRefPubMed
30.
go back to reference Fernandez, Christine, Marion Buyse, Michèle German-Fattal, and François Gimenez. 2004. Influence of the pro-inflammatory cytokines on P-glycoprotein expression and functionality. Journal of Pharmacy & Pharmaceutical Sciences : a publication of the Canadian Society for Pharmaceutical Sciences, Societe canadienne des sciences pharmaceutiques 7: 359–371. Fernandez, Christine, Marion Buyse, Michèle German-Fattal, and François Gimenez. 2004. Influence of the pro-inflammatory cytokines on P-glycoprotein expression and functionality. Journal of Pharmacy & Pharmaceutical Sciences : a publication of the Canadian Society for Pharmaceutical Sciences, Societe canadienne des sciences pharmaceutiques 7: 359–371.
31.
go back to reference Le Vee, Marc, Philippe Gripon, Bruno Stieger, and Olivier Fardel. 2008. Down-regulation of organic anion transporter expression in human hepatocytes exposed to the proinflammatory cytokine interleukin 1beta. Drug Metabolism and Disposition: The Biological Fate of Chemicals 36: 217–222. https://doi.org/10.1124/dmd.107.016907.CrossRef Le Vee, Marc, Philippe Gripon, Bruno Stieger, and Olivier Fardel. 2008. Down-regulation of organic anion transporter expression in human hepatocytes exposed to the proinflammatory cytokine interleukin 1beta. Drug Metabolism and Disposition: The Biological Fate of Chemicals 36: 217–222. https://​doi.​org/​10.​1124/​dmd.​107.​016907.CrossRef
33.
35.
go back to reference Campion, Sarah N., Rachel Johnson, Lauren M. Aleksunes, Michael J. Goedken, Nico van Rooijen, George L. Scheffer, Nathan J. Cherrington, and José E. Manautou. 2008. Hepatic Mrp4 induction following acetaminophen exposure is dependent on Kupffer cell function. American Journal of Physiology-Gastrointestinal and Liver Physiology. American Physiological Society 295: G294–G304. https://doi.org/10.1152/ajpgi.00541.2007.CrossRefPubMedPubMedCentral Campion, Sarah N., Rachel Johnson, Lauren M. Aleksunes, Michael J. Goedken, Nico van Rooijen, George L. Scheffer, Nathan J. Cherrington, and José E. Manautou. 2008. Hepatic Mrp4 induction following acetaminophen exposure is dependent on Kupffer cell function. American Journal of Physiology-Gastrointestinal and Liver Physiology. American Physiological Society 295: G294–G304. https://​doi.​org/​10.​1152/​ajpgi.​00541.​2007.CrossRefPubMedPubMedCentral
36.
go back to reference Song, Im-Sook, In-Kyoung Lee, Suk-Jae Chung, Sang-Geon Kim, Myung-Gull Lee, and Chang-Koo Shim. 2002. Effect of nitric oxide on the sinusoidal uptake of organic cations and anions by isolated hepatocytes. Archives of Pharmacal Research 25: 984–988.CrossRef Song, Im-Sook, In-Kyoung Lee, Suk-Jae Chung, Sang-Geon Kim, Myung-Gull Lee, and Chang-Koo Shim. 2002. Effect of nitric oxide on the sinusoidal uptake of organic cations and anions by isolated hepatocytes. Archives of Pharmacal Research 25: 984–988.CrossRef
37.
go back to reference Cha, Seok Ho, Hong Pyo Kim, Nam-Hee Jung, Woon Ki Lee, Ju Young Kim, and Young-Nam Cha. 2002. Down-regulation of organic anion transporter 2 mRNA expression by nitric oxide in primary cultured rat hepatocytes. IUBMB Life (International Union of Biochemistry and Molecular Biology: Life) 54: 129–135. https://doi.org/10.1080/15216540214534.CrossRef Cha, Seok Ho, Hong Pyo Kim, Nam-Hee Jung, Woon Ki Lee, Ju Young Kim, and Young-Nam Cha. 2002. Down-regulation of organic anion transporter 2 mRNA expression by nitric oxide in primary cultured rat hepatocytes. IUBMB Life (International Union of Biochemistry and Molecular Biology: Life) 54: 129–135. https://​doi.​org/​10.​1080/​15216540214534.CrossRef
40.
go back to reference Morgan, E.T. 2001. Regulation of cytochrome p450 by inflammatory mediators: Why and how? Drug Metabolism and Disposition: The Biological Fate of Chemicals 29: 207–212. Morgan, E.T. 2001. Regulation of cytochrome p450 by inflammatory mediators: Why and how? Drug Metabolism and Disposition: The Biological Fate of Chemicals 29: 207–212.
42.
go back to reference Conforti, A., S. Lussignoli, S. Bertani, R. Ortolani, L. Cuzzolin, G. Benoni, and P. Bellavite. 2019. Cytokine and nitric oxide levels in a rat model of immunologic protection from adjuvant-induced arthritis. International Journal of Immunopathology and Pharmacology 14: 153–160 http://www.ncbi.nlm.nih.gov/pubmed/12604016. Accessed June 28. Conforti, A., S. Lussignoli, S. Bertani, R. Ortolani, L. Cuzzolin, G. Benoni, and P. Bellavite. 2019. Cytokine and nitric oxide levels in a rat model of immunologic protection from adjuvant-induced arthritis. International Journal of Immunopathology and Pharmacology 14: 153–160 http://​www.​ncbi.​nlm.​nih.​gov/​pubmed/​12604016. Accessed June 28.
43.
go back to reference Koss, McKenzie, Gordon R. Pfeiffer, Ying Wang, Sharon T. Thomas, Michael Yerukhimovich, William A. Gaarde, Claire M. Doerschuk, and Qin Wang. 2006. Ezrin/radixin/moesin proteins are phosphorylated by TNF-alpha and modulate permeability increases in human pulmonary microvascular endothelial cells. Journal of Immunology (Baltimore, Md. : 1950) 176: 1218–1227. https://doi.org/10.4049/jimmunol.176.2.1218.CrossRef Koss, McKenzie, Gordon R. Pfeiffer, Ying Wang, Sharon T. Thomas, Michael Yerukhimovich, William A. Gaarde, Claire M. Doerschuk, and Qin Wang. 2006. Ezrin/radixin/moesin proteins are phosphorylated by TNF-alpha and modulate permeability increases in human pulmonary microvascular endothelial cells. Journal of Immunology (Baltimore, Md. : 1950) 176: 1218–1227. https://​doi.​org/​10.​4049/​jimmunol.​176.​2.​1218.CrossRef
45.
go back to reference Amoozadeh, Yasaman, Qinghong Dan, Jenny Xiao, Faiza Waheed, and Katalin Szászi. 2015. Tumor necrosis factor-α induces a biphasic change in claudin-2 expression in tubular epithelial cells: role in barrier functions. American Journal of Physiology 309. Cell Physiology. American Physiological Society: C38–C50. https://doi.org/10.1152/ajpcell.00388.2014.CrossRefPubMed Amoozadeh, Yasaman, Qinghong Dan, Jenny Xiao, Faiza Waheed, and Katalin Szászi. 2015. Tumor necrosis factor-α induces a biphasic change in claudin-2 expression in tubular epithelial cells: role in barrier functions. American Journal of Physiology 309. Cell Physiology. American Physiological Society: C38–C50. https://​doi.​org/​10.​1152/​ajpcell.​00388.​2014.CrossRefPubMed
46.
go back to reference Schmidt, Christian, Bailu Peng, Zhongkui Li, Guido M. Sclabas, Shuichi Fujioka, Jiangong Niu, Marc Schmidt-Supprian, Douglas B. Evans, James L. Abbruzzese, and Paul J. Chiao. 2003. Mechanisms of proinflammatory cytokine-induced biphasic NF-kappaB activation. Molecular Cell 12: 1287–1300.CrossRef Schmidt, Christian, Bailu Peng, Zhongkui Li, Guido M. Sclabas, Shuichi Fujioka, Jiangong Niu, Marc Schmidt-Supprian, Douglas B. Evans, James L. Abbruzzese, and Paul J. Chiao. 2003. Mechanisms of proinflammatory cytokine-induced biphasic NF-kappaB activation. Molecular Cell 12: 1287–1300.CrossRef
47.
go back to reference Yano, Kentaro, Takumi Tomono, Riyo Sakai, Takashi Kano, Kaori Morimoto, Yukio Kato, and Takuo Ogihara. 2013. Contribution of radixin to P-glycoprotein expression and transport activity in mouse small intestine in vivo. Journal of Pharmaceutical Sciences 102: 2875–2881. https://doi.org/10.1002/jps.23637.CrossRefPubMed Yano, Kentaro, Takumi Tomono, Riyo Sakai, Takashi Kano, Kaori Morimoto, Yukio Kato, and Takuo Ogihara. 2013. Contribution of radixin to P-glycoprotein expression and transport activity in mouse small intestine in vivo. Journal of Pharmaceutical Sciences 102: 2875–2881. https://​doi.​org/​10.​1002/​jps.​23637.CrossRefPubMed
48.
go back to reference Yano, Kentaro, Kyoma Otsuka, Yuko Kato, Hideaki Kawabata, Shinya Ohmori, Hiroshi Arakawa, and Takuo Ogihara. 2016. Different regulation of P-glycoprotein function between Caco-2 and Caki-1 cells by ezrin, radixin and moesin proteins. Journal of Pharmacy and Pharmacology 68: 361–367. https://doi.org/10.1111/jphp.12525.CrossRefPubMed Yano, Kentaro, Kyoma Otsuka, Yuko Kato, Hideaki Kawabata, Shinya Ohmori, Hiroshi Arakawa, and Takuo Ogihara. 2016. Different regulation of P-glycoprotein function between Caco-2 and Caki-1 cells by ezrin, radixin and moesin proteins. Journal of Pharmacy and Pharmacology 68: 361–367. https://​doi.​org/​10.​1111/​jphp.​12525.CrossRefPubMed
50.
go back to reference Hegedüs, Tamás, Tamás Sessler, Robert Scott, William Thelin, Éva Bakos, András Váradi, Katalin Szabó, László Homolya, Sharon L. Milgram, and Balázs Sarkadi. 2003. C-terminal phosphorylation of MRP2 modulates its interaction with PDZ proteins. Biochemical and Biophysical Research Communications 302: 454–461. https://doi.org/10.1016/S0006-291X(03)00196-7.CrossRefPubMed Hegedüs, Tamás, Tamás Sessler, Robert Scott, William Thelin, Éva Bakos, András Váradi, Katalin Szabó, László Homolya, Sharon L. Milgram, and Balázs Sarkadi. 2003. C-terminal phosphorylation of MRP2 modulates its interaction with PDZ proteins. Biochemical and Biophysical Research Communications 302: 454–461. https://​doi.​org/​10.​1016/​S0006-291X(03)00196-7.CrossRefPubMed
51.
Metadata
Title
Changes in Radixin Expression and Interaction with Efflux Transporters in the Liver of Adjuvant-Induced Arthritic Rats
Authors
Atsushi Kawase
Misaki Nakasaka
Hatsune Bando
Saori Yasuda
Hiroaki Shimada
Masahiro Iwaki
Publication date
01-02-2020
Publisher
Springer US
Published in
Inflammation / Issue 1/2020
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-019-01097-9

Other articles of this Issue 1/2020

Inflammation 1/2020 Go to the issue