Expression patterns of nuclear receptors in parenchymal and non-parenchymal mouse liver cells and their modulation in cholestasis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1863, Issue 7, 2017, Pages 1699-1708

  Gonzalez Sanchez, Ester ^a   Firrincieli, Delphine ^a   Housset, Chantal ^a,b   Chignard, Nicolas ^a,c  

^a SORBONNE UNIVERSITÉ   (France)

^b HÔPITAL SAINT ANTOINE   (France)

^c Inovarion   (France)

Author keywords

Abcb4 knockout mice; Bile duct ligation; Hepatocytes; Non parenchymal liver cells

Indexed keywords

CELL NUCLEUS RECEPTOR; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 1; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; CYTOCHROME P450 3A11; ESTROGEN RECEPTOR ALPHA; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PROGESTERONE RECEPTOR; TRANSCRIPTOME; VASCULAR CELL ADHESION MOLECULE 1; ABC TRANSPORTER SUBFAMILY B; CELL RECEPTOR; P-GLYCOPROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; CELL ISOLATION; CHOLANGIOCYTE; CONTROLLED STUDY; EXPERIMENTAL CHOLESTASIS; HEPATIC STELLATE CELL; KUPFFER CELL; LIPID METABOLISM; LIVER CELL; LIVER CELL DAMAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCLEROSING CHOLANGITIS; UPREGULATION; ANIMAL; BIOSYNTHESIS; CHOLESTASIS; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM; PATHOLOGY;

ANIMALS; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY B; CHOLESTASIS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HEPATOCYTES; LIVER; MICE; MICE, KNOCKOUT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTOME;

EID: 85019373819     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2017.04.004     Document Type: Article

References (48)

1. [1] Mangelsdorf, D.J., Thummel, C., Beato, M., Herrlich, P., Schutz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., Evans, R.M., The nuclear receptor superfamily: the second decade. Cell 83 (1995), 835–839.
2. [2] Bookout, A.L., Jeong, Y., Downes, M., Yu, R.T., Evans, R.M., Mangelsdorf, D.J., Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126 (2006), 789–799.
3. [3] Gofflot, F., Chartoire, N., Vasseur, L., Heikkinen, S., Dembele, D., Le Merrer, J., Auwerx, J., Systematic gene expression mapping clusters nuclear receptors according to their function in the brain. Cell 131 (2007), 405–418.
4. [4] Chuang, J.C., Cha, J.Y., Garmey, J.C., Mirmira, R.G., Repa, J.J., Research resource: nuclear hormone receptor expression in the endocrine pancreas. Mol. Endocrinol. 22 (2008), 2353–2363.
5. [5] Modica, S., Gofflot, F., Murzilli, S., D'Orazio, A., Salvatore, L., Pellegrini, F., Nicolucci, A., Tognoni, G., Copetti, M., Valanzano, R., Veschi, S., Mariani-Costantini, R., Palasciano, G., Schoonjans, K., Auwerx, J., Moschetta, A., The intestinal nuclear receptor signature with epithelial localization patterns and expression modulation in tumors. Gastroenterology 138 (2010), 636–648 (648 e631–612).
6. [6] Vacca, M., D'Amore, S., Graziano, G., D'Orazio, A., Cariello, M., Massafra, V., Salvatore, L., Martelli, N., Murzilli, S., Lo Sasso, G., Mariani-Costantini, R., Moschetta, A., Clustering nuclear receptors in liver regeneration identifies candidate modulators of hepatocyte proliferation and hepatocarcinoma. PLoS One, 9, 2014, e104449.
7. [7] Wagner, M., Zollner, G., Trauner, M., Nuclear receptors in liver disease. Hepatology 53 (2011), 1023–1034.
8. [8] Halilbasic, E., Baghdasaryan, A., Trauner, M., Nuclear receptors as drug targets in cholestatic liver diseases. Clin. Liver Dis. 17 (2013), 161–189.
9. [9] Li, Z., Kruijt, J.K., van der Sluis, R.J., Van Berkel, T.J., Hoekstra, M., Nuclear receptor atlas of female mouse liver parenchymal, endothelial, and Kupffer cells. Physiol. Genomics 45 (2013), 268–275.
10. [10] D'Aldebert, E., Biyeyeme Bi Mve, M.J., Mergey, M., Wendum, D., Firrincieli, D., Coilly, A., Fouassier, L., Corpechot, C., Poupon, R., Housset, C., Chignard, N., Bile salts control the antimicrobial peptide cathelicidin through nuclear receptors in the human biliary epithelium. Gastroenterology 136 (2009), 1435–1443.
11. [11] Firrincieli, D., Zuniga, S., Rey, C., Wendum, D., Lasnier, E., Rainteau, D., Braescu, T., Falguieres, T., Boissan, M., Cadoret, A., Housset, C., Chignard, N., Vitamin D nuclear receptor deficiency promotes cholestatic liver injury by disruption of biliary epithelial cell junctions in mice. Hepatology 58 (2013), 1401–1412.
12. [12] Ding, N., Yu, R.T., Subramaniam, N., Sherman, M.H., Wilson, C., Rao, R., Leblanc, M., Coulter, S., He, M., Scott, C., Lau, S.L., Atkins, A.R., Barish, G.D., Gunton, J.E., Liddle, C., Downes, M., Evans, R.M., A vitamin D receptor/SMAD genomic circuit gates hepatic fibrotic response. Cell 153 (2013), 601–613.
13. [13] Hochrath, K., Stokes, C.S., Geisel, J., Pollheimer, M.J., Fickert, P., Dooley, S., Lammert, F., Vitamin D modulates biliary fibrosis in ABCB4-deficient mice. Hepatol. Int. 8 (2014), 443–452.
14. [14] Reiter, F.P., Hohenester, S., Nagel, J.M., Wimmer, R., Artmann, R., Wottke, L., Makeschin, M.C., Mayr, D., Rust, C., Trauner, M., Denk, G.U., 1,25-(OH)(2)-vitamin D(3) prevents activation of hepatic stellate cells in vitro and ameliorates inflammatory liver damage but not fibrosis in the Abcb4(−/−) model. Biochem. Biophys. Res. Commun. 459 (2015), 227–233.
15. [15] Gascon-Barre, M., Demers, C., Mirshahi, A., Neron, S., Zalzal, S., Nanci, A., The normal liver harbors the vitamin D nuclear receptor in nonparenchymal and biliary epithelial cells. Hepatology 37 (2003), 1034–1042.
16. [16] Gonzalez-Sanchez, E., Firrincieli, D., Housset, C., Chignard, N., Nuclear receptors in acute and chronic cholestasis. Dig. Dis. 33 (2015), 357–366.
17. [17] Yang, X., Downes, M., Yu, R.T., Bookout, A.L., He, W., Straume, M., Mangelsdorf, D.J., Evans, R.M., Nuclear receptor expression links the circadian clock to metabolism. Cell 126 (2006), 801–810.
18. [18] Lemoinne, S., Cadoret, A., Rautou, P.E., El Mourabit, H., Ratziu, V., Corpechot, C., Rey, C., Bosselut, N., Barbu, V., Wendum, D., Feldmann, G., Boulanger, C., Henegar, C., Housset, C., Thabut, D., Portal myofibroblasts promote vascular remodeling underlying cirrhosis formation through the release of microparticles. Hepatology 61 (2015), 1041–1055.
19. [19] Fu, M., Sun, T., Bookout, A.L., Downes, M., Yu, R.T., Evans, R.M., Mangelsdorf, D.J., A nuclear receptor atlas: 3T3-L1 adipogenesis. Mol. Endocrinol. 19 (2005), 2437–2450.
20. [20] Bookout, A.L., Cummins, C.L., Mangelsdorf, D.J., Pesola, J.M., Kramer, M.F., Ausubel, Frederick M. High-throughput real-time quantitative reverse transcription PCR, current protocols in molecular biology, 2006 Chapter 15. (Unit 15 18).
21. [21] Metsalu, T., Vilo, J., ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 43 (2015), W566–W570.
22. [22] Kakhniashvili, D.G., Bulla, L.A. Jr., Goodman, S.R., The human erythrocyte proteome: analysis by ion trap mass spectrometry. Mol. Cell. Proteomics 3 (2004), 501–509.
23. [23] Chai, J., Luo, D., Wu, X., Wang, H., He, Y., Li, Q., Zhang, Y., Chen, L., Peng, Z.H., Xiao, T., Wang, R., Chen, W., Changes of organic anion transporter MRP4 and related nuclear receptors in human obstructive cholestasis. J. Gastrointest. Surg. 15 (2011), 996–1004.
24. [24] Demeilliers, C., Jacquemin, E., Barbu, V., Mergey, M., Paye, F., Fouassier, L., Chignard, N., Housset, C., Lomri, N.E., Altered hepatobiliary gene expressions in PFIC1: ATP8B1 gene defect is associated with CFTR downregulation. Hepatology 43 (2006), 1125–1134.
25. [25] Zollner, G., Wagner, M., Fickert, P., Silbert, D., Gumhold, J., Zatloukal, K., Denk, H., Trauner, M., Expression of bile acid synthesis and detoxification enzymes and the alternative bile acid efflux pump MRP4 in patients with primary biliary cirrhosis. Liver Int. 27 (2007), 920–929.
26. [26] Chen, H.L., Liu, Y.J., Wu, S.H., Ni, Y.H., Ho, M.C., Lai, H.S., Hsu, W.M., Hsu, H.Y., Tseng, H.C., Jeng, Y.M., Chang, M.H., Expression of hepatocyte transporters and nuclear receptors in children with early and late-stage biliary atresia. Pediatr. Res. 63 (2008), 667–673.
27. [27] Georgiev, P., Jochum, W., Heinrich, S., Jang, J.H., Nocito, A., Dahm, F., Clavien, P.A., Characterization of time-related changes after experimental bile duct ligation. Br. J. Surg. 95 (2008), 646–656.
28. [28] Ikenaga, N., Liu, S.B., Sverdlov, D.Y., Yoshida, S., Nasser, I., Ke, Q., Kang, P.M., Popov, Y., A new Mdr2(−/−) mouse model of sclerosing cholangitis with rapid fibrosis progression, early-onset portal hypertension, and liver cancer. Am. J. Pathol. 185 (2015), 325–334.
29. [29] Doignon, I., Julien, B., Serriere-Lanneau, V., Garcin, I., Alonso, G., Nicou, A., Monnet, F., Gigou, M., Humbert, L., Rainteau, D., Azoulay, D., Castaing, D., Gillon, M.C., Samuel, D., Duclos-Vallee, J.C., Tordjmann, T., Immediate neuroendocrine signaling after partial hepatectomy through acute portal hyperpressure and cholestasis. J. Hepatol. 54 (2011), 481–488.
30. [30] Galli, A., Crabb, D., Price, D., Ceni, E., Salzano, R., Surrenti, C., Casini, A., Peroxisome proliferator-activated receptor gamma transcriptional regulation is involved in platelet-derived growth factor-induced proliferation of human hepatic stellate cells. Hepatology 31 (2000), 101–108.
31. [31] Marra, F., Efsen, E., Romanelli, R.G., Caligiuri, A., Pastacaldi, S., Batignani, G., Bonacchi, A., Caporale, R., Laffi, G., Pinzani, M., Gentilini, P., Ligands of peroxisome proliferator-activated receptor gamma modulate profibrogenic and proinflammatory actions in hepatic stellate cells. Gastroenterology 119 (2000), 466–478.
32. [32] Miyahara, T., Schrum, L., Rippe, R., Xiong, S., Yee, H.F. Jr., Motomura, K., Anania, F.A., Willson, T.M., Tsukamoto, H., Peroxisome proliferator-activated receptors and hepatic stellate cell activation. J. Biol. Chem. 275 (2000), 35715–35722.
33. [33] She, H., Xiong, S., Hazra, S., Tsukamoto, H., Adipogenic transcriptional regulation of hepatic stellate cells. J. Biol. Chem. 280 (2005), 4959–4967.
34. [34] Yi, S.H., Zhang, Y., Tang, D., Zhu, L., Mechanical force and tensile strain activated hepatic stellate cells and inhibited retinol metabolism. Biotechnol. Lett. 37 (2015), 1141–1152.
35. [35] Kinnman, N., Goria, O., Wendum, D., Gendron, M.C., Rey, C., Poupon, R., Housset, C., Hepatic stellate cell proliferation is an early platelet-derived growth factor-mediated cellular event in rat cholestatic liver injury. Lab. Investig. 81 (2001), 1709–1716.
36. [36] Fickert, P., Fuchsbichler, A., Moustafa, T., Wagner, M., Zollner, G., Halilbasic, E., Stoger, U., Arrese, M., Pizarro, M., Solis, N., Carrasco, G., Caligiuri, A., Sombetzki, M., Reisinger, E., Tsybrovskyy, O., Zatloukal, K., Denk, H., Jaeschke, H., Pinzani, M., Trauner, M., Farnesoid X receptor critically determines the fibrotic response in mice but is expressed to a low extent in human hepatic stellate cells and periductal myofibroblasts. Am. J. Pathol. 175 (2009), 2392–2405.
37. [37] Fiorucci, S., Antonelli, E., Rizzo, G., Renga, B., Mencarelli, A., Riccardi, L., Orlandi, S., Pellicciari, R., Morelli, A., The nuclear receptor SHP mediates inhibition of hepatic stellate cells by FXR and protects against liver fibrosis. Gastroenterology 127 (2004), 1497–1512.
38. [38] Duez, H., van der Veen, J.N., Duhem, C., Pourcet, B., Touvier, T., Fontaine, C., Derudas, B., Bauge, E., Havinga, R., Bloks, V.W., Wolters, H., van der Sluijs, F.H., Vennstrom, B., Kuipers, F., Staels, B., Regulation of bile acid synthesis by the nuclear receptor Rev-erbalpha. Gastroenterology 135 (2008), 689–698.
39. [39] Le Martelot, G., Claudel, T., Gatfield, D., Schaad, O., Kornmann, B., Lo Sasso, G., Moschetta, A., Schibler, U., REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol., 7, 2009, e1000181.
40. [40] Moustafa, T., Fickert, P., Magnes, C., Guelly, C., Thueringer, A., Frank, S., Kratky, D., Sattler, W., Reicher, H., Sinner, F., Gumhold, J., Silbert, D., Fauler, G., Hofler, G., Lass, A., Zechner, R., Trauner, M., Alterations in lipid metabolism mediate inflammation, fibrosis, and proliferation in a mouse model of chronic cholestatic liver injury. Gastroenterology 142 (2012), 140–151 (e112).
41. [41] Mataki, C., Magnier, B.C., Houten, S.M., Annicotte, J.S., Argmann, C., Thomas, C., Overmars, H., Kulik, W., Metzger, D., Auwerx, J., Schoonjans, K., Compromised intestinal lipid absorption in mice with a liver-specific deficiency of liver receptor homolog 1. Mol. Cell. Biol. 27 (2007), 8330–8339.
42. [42] Carey, E.J., Ali, A.H., Lindor, K.D., Primary biliary cirrhosis. Lancet 386 (2015), 1565–1575.
43. [43] van Nieuwerk, C.M., Groen, A.K., Ottenhoff, R., van Wijland, M., van den Bergh Weerman, M.A., Tytgat, G.N., Offerhaus, J.J., Oude Elferink, R.P., The role of bile salt composition in liver pathology of mdr2 (−/−) mice: differences between males and females. J. Hepatol. 26 (1997), 138–145.
44. [44] Lu, Y.F., Jin, T., Xu, Y., Zhang, D., Wu, Q., Zhang, Y.K., Liu, J., Sex differences in the circadian variation of cytochrome p450 genes and corresponding nuclear receptors in mouse liver. Chronobiol. Int. 30 (2013), 1135–1143.
45. [45] Sun, J., Kong, J., Duan, Y., Szeto, F.L., Liao, A., Madara, J.L., Li, Y.C., Increased NF-kappaB activity in fibroblasts lacking the vitamin D receptor. Am. J. Physiol. Endocrinol. Metab. 291 (2006), E315–E322.
46. [46] Zhao, Y., Bruemmer, D., NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology. Arterioscler. Thromb. Vasc. Biol. 30 (2010), 1535–1541.
47. [47] Rosmorduc, O., Housset, C., Hypoxia: a link between fibrogenesis, angiogenesis, and carcinogenesis in liver disease. Semin. Liver Dis. 30 (2010), 258–270.
48. [48] Rosmorduc, O., Wendum, D., Corpechot, C., Galy, B., Sebbagh, N., Raleigh, J., Housset, C., Poupon, R., Hepatocellular hypoxia-induced vascular endothelial growth factor expression and angiogenesis in experimental biliary cirrhosis. Am. J. Pathol. 155 (1999), 1065–1073.