Mechanisms of oxysterol-induced disease: insights from the biliary system

References

• Jusakul A, Yongvanit P, Loilome W, Namwat N, Kuver R. Mechanisms of oxysterol-induced carcinogenesis. Lipids Health Dis. 10, 44 (2011).
   Google Scholar
• Otaegui-Arrazola A, Menendez-Carreno M, Ansorena D, Astiasaran I. Oxysterols: a world to explore. Food Chem. Toxicol. 48, 3289–3303 (2010).
   Google Scholar
• Hovenkamp E, Demonty I, Plat J, Lutjohann D, Mensink RP, Trautwein EA. Biological effects of oxidized phytosterols: a review of the current knowledge. Prog. Lipid Res. 47, 37–49 (2008).
   Google Scholar
• Guardiola F, Codony R, Addis PB, Rafecas M, Boatella J. Biological effects of oxysterols: current status. Food Chem. Toxicol. 34, 193–211 (1996).
   Google Scholar
• Sottero B, Gamba P, Gargiulo S, Leonarduzzi G, Poli G. Cholesterol oxidation products and disease: an emerging topic of interest in medicinal chemistry. Curr. Med. Chem. 16, 685–705 (2009).
   Google Scholar
• Vejux A, Lizard G. Cytotoxic effects of oxysterols associated with human diseases: induction of cell death (apoptosis and/or oncosis), oxidative and inflammatory activities, and phospholipidosis. Mol. Aspects Med. 30, 153–170 (2009).
   Google Scholar
• Schroepfer GJ Jr. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 80, 361–554 (2000).
   Google Scholar
• Smith LL. Cholesterol Autoxidation. Plenum Press, NY, USA (1981).
   Google Scholar
• Wollam J, Antebi A. Sterol regulation of metabolism, homeostasis, and development. Annu. Rev. Biochem. 80, 885–916 (2011).
   Google Scholar
• Javitt NB. Oxysterols: novel biologic roles for the 21st century. Steroids 73, 149–157 (2008).
   Google Scholar
• Crosignani A, Zuin M, Allocca M, Del Puppo M. Oxysterols in bile acid metabolism. Clin. Chim. Acta 412, 2037–2045 (2011).
   Google Scholar
• Shibata N, Glass CK. Macrophages, oxysterols and atherosclerosis. Circulation J. 74, 2045–2051 (2010).
   Google Scholar
• Diczfalusy U. Analysis of cholesterol oxidation products in biological samples. J. AOAC Int. 87, 467–473 (2004).
   Google Scholar
• Wu Z, Martin KO, Javitt NB, Chiang JY. Structure and functions of human oxysterol 7a-hydroxylase cDNAs and gene CYP7B1. J. Lipid Res. 40, 2195–2203 (1999).
   Google Scholar
• Russell DW. Oxysterol biosynthetic enzymes. Biochim. Biophys. Acta 1529, 126–135 (2000).
   Google Scholar
• Brown AJ, Jessup W. Oxysterols: sources, cellular storage and metabolism and new insights into their roles in cholesterol homeostasis. Mol. Aspects Med. 30, 111–122 (2009).
   Google Scholar
• Bjorkhem I, Lutjohann D, Diczfalusky U, Stahle L, Ahlborg G, Wahren J. Cholesterol homeostasis in human brain: turnover of 24(S)-hydroxycholesterol and evidence for a cerebral origin of most of this oxysterol in the circulation. J. Lipid Res. 39, 1594–1600 (1998).
   Google Scholar
• Iuliano L. Pathways of cholesterol oxidation via non-enzymatic mechanisms. Chem. Phys. Lipids 164, 457–468 (2011).
   Google Scholar
• McDonald JG, Smith DD, Stiles AR, Russell DW. A comprehensive method for extraction and quantitative analysis of sterols and secosteroids from human plasma. J. Lipid Res. 53, 1399–1409 (2012).
   Google Scholar
• Xu L, Sheflin LG, Poter NA, Fliesler SJ. 7-dehydrocholesterol-derived oxysterols and retinal degeneration in a rat model of Smith–Lemli–Opitz syndrome. Biochim. Biophys. Acta 1821(6), 877–883 (2012).
   Google Scholar
• Haigh WG, Lee SP. Identification of oxysterols in human bile and pigment gallstones. Gastroenterology 121, 118–123 (2001). ▪▪ First description of oxysterol species in human bile and pigment gallstones.
   Google Scholar
• Yoshida T, Matsuzaki Y, Haigh WG et al. Origin of oxysterols in hepatic bile of patients with biliary infection. Am. J. Gastroenterol. 98, 2275–2280 (2003). ▪▪ Comprehensive quantitative analysis of oxysterol species in hepatic bile obtained from patients with biliary tract diseases, showing an association with infected bile.
   Google Scholar
• Iuliano L, Michelette F, Natoli S, Ginanni Corradini S et al. Measurement of oxysterols and alpha-tocopherol in plasma and tissue samples as indices of oxidant stress status. Anal. Biochem. 312, 217–223 (2003).
   Google Scholar
• Kidambi S, Patel SB. Cholesterol and non-cholesterol sterol transporters: ABCG5, ABCG8 and NPC1L1: a review. Xenobiotica 38, 1119–1139 (2008).
   Google Scholar
• Staprans I, Pan XM, Rapp JH, Feingold KR. Oxidized cholesterol in the diet is a source of oxidized lipoproteins in human serum. J. Lipid Res. 44, 705–715 (2003).
   Google Scholar
• Liseisen J, Wolfram G. Absorption of cholesterol oxidation products from ordinary foodstuff in humans. Ann. Nutr. Metab. 42, 221–230 (1998).
   Google Scholar
• Brown MS, Goldstein JL. Cholesterol feedback: from Schoenheimer’s bottle to Scap’s MELADL. J. Lipid Res. 50(Suppl.), S15–S27 (2009).
   Google Scholar
• Gill S, Chow R, Brown AJ. Sterol regulators of cholesterol homeostasis and beyond: the oxysterol hypothesis revisited and revised. Prog. Lipid Res. 47, 391–404 (2008).
   Google Scholar
• Lange Y, Ory DS, Ye J, Lanier MH, Hsu FF, Seck TL. Effectors of rapid homeostatic responses of endoplasmic reticulum cholesterol and HMG-CoA reductase. J. Biol Chem. 283, 1445–1455 (2008).
   Google Scholar
• Porter JA. Cholesterol modification of hedgehog signaling proteins in animal development. Science 274, 255–259 (1996).
   Google Scholar
• Mann RK, Beachy PA. Novel lipid modifications of secreted protein signals. Annu. Rev. Biochem. 73, 891–923 (2004).
   Google Scholar
• Stottmann RW, Turbe-Doan A, Tran P et al. Cholesterol metabolism is required for intracellular hedgehog signal transduction in vivo. PLoS Genet. 7, e1002224 (2011).
   Google Scholar
• Kha HT, Basseri B, Shouhed D et al. Oxysterols regulate differentiation of mesenchymal stem cells: pro-bone and anti-fat. J. Bone Miner. Res. 19, 830–840 (2004).
   Google Scholar
• Dwyer JR, Sever N, Carlson M, Nelson SF, Beachy PA, Parhami F. Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. J. Biol Chem. 282, 8959–8968 (2007).
   Google Scholar
• Corcoran RB, Scott MP. Oxysterols stimulate Sonic hedgehog signal transduction and proliferation of medulloblastoma cells. Proc. Natl Acad. Sci. USA 103, 8408–8413 (2006).
   Google Scholar
• Nachtergaele S, Mydock LK, Krishnan K et al. Oxysterols are allosteric activators of the oncoprotein Smoothened. Nat. Chem. Biol. 8, 211–220 (2012).
   Google Scholar
• Hannedouche S, Zhang J, Yi T et al. Oxysterols direct B cell and T cell migration via EBI2. Nature 475, 524–527 (2011).
   Google Scholar
• Liu C, Yang XV, Wu J et al. Oxysterols direct B-cell migration through EBI2. Nature 475, 519–523 (2011).
   Google Scholar
• Ngo MH, Colbourne TR, Ridgway ND. Functional implications of sterol transport by the oxysterol-binding protein gene family. Biochem. J. 429, 13–24 (2010).
   Google Scholar
• Lehto M, Olkkonen VM. The OSBP-related proteins: a novel protein family involved in vesicle transport, cellular lipid metabolism and cell signaling. Biochim. Biophys. Acta 1631, 1–11 (2003).
   Google Scholar
• Raychaudhuri S, Prinz WA. The diverse functions of oxysterol-binding proteins. Annu. Rev. Cell Dev. Biol. 26, 157–177 (2010).
   Google Scholar
• Ryan E, Chopra J, McCarthy FO, Maguire AR, O’Brien NM. Qualitative and quantitative comparison of the cytotoxic and apoptotic potential of phytosterol and oxidation products with their corresponding cholesterol oxidation products. Br. J. Nutr. 94, 443–451 (2005).
   Google Scholar
• Bjorkhem I, Diczfalusy U. Oxysterols: friends, foes, or just fellow passengers? Arterioscler. Thromb. Vasc. Biol. 22. 734–742 (2002).
   Google Scholar
• Kudo K, Emmons GT, Casserly EW et al. Inhibitors of sterol synthesis. Chromatography of acetate derivatives of oxygenated sterols. J. Lipid Res. 30, 1097–1111 (1989).
   Google Scholar
• Fuda H, Javitt NB, Mitamura K, Ikegawa S, Strott CA. Oxysterols are substrates for cholesterol sulfotransferase. J. Lipid Res. 48, 1343–1352 (2007).
   Google Scholar
• Xu L, Bai Q, Rodriguez-Agudo D, Hylemon P et al. Regulation of hepatocyte lipid metabolism and inflammatory response by 25-hydroxycholeserol and 25-hydroxycholesterol-3-sulfate. Lipids 45, 821–832 (2010).
   Google Scholar
• Bai Q, Xu L, Kakiyama G, Runge-Morris MA, Hylemon P et al. Sulfation of 25-hydroxycholesterol by SULF2B1b decreases cellular lipids via the LXR/ SREBP-1c signaling pathway in human aortic endothelial cells. Atherosclerosis 214, 350–356 (2011).
   Google Scholar
• Xu L, Shen S, Ma Y et al. 25-hydroxycholesterol-3-sulfate attenuates inflammatory response via PPARg signaling in human THP-1 macrophages. Am. J. Physiol. Endocrinol. Metab. 302, e788–e799 (2012).
   Google Scholar
• Bai Q, Zhang X, Xu L et al. Oxysterol sulfation by cytosolic sulfotransferase suppresses liver X receptor/sterol regulatory element binding protein-1c signaling pathway and reduces serum and hepatic lipids in mouse models of nonalcoholic fatty liver disease. Metabolism 61, 836–845 (2012).
   Google Scholar
• Ko CW, Lee SP. Gallstone formation. Local factors. Gastroenterol. Clin. North Am. 28, 99–115 (1999).
   Google Scholar
• Stokes CS, Krawczyk M, Lammert F. Gallstones: environment, lifestyle and genes. Dig. Dis. 29, 191–201 (2011).
   Google Scholar
• Lee DK, Tarr PI, Haigh WG, Lee SP. Bacterial DNA in mixed cholesterol gallstones. Am. J. Gastroenterol. 94, 3502–3506 (1999).
   Google Scholar
• Haigh WG, Wong T, Lee SP. The production of oxysterols in bile by activated human leukocytes. Biochem. Biophys. Res. Comm. 34, 467–469 (2006).
   Google Scholar
• Oda D, Lee SP, Hayashi A. Long-term culture and partial characterization of dog gallbladder epithelial cells. Lab. Invest. 64, 682–692 (1991).
   Google Scholar
• Seo DW, Choi H-S, Lee SP, Kuver R. Oxysterols from human bile induce apoptosis of canine gallbladder epithelial cells in monolayer culture. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G1247–G1256 (2004). ▪ Cultured dog gallbladder epithelial cells were found to undergo apoptosis via a mitochondrial pathway when exposed to model bile solutions containing cholest-4-en-3-one, cholesta-4,6-dien-3-one, and 5b-cholestan-3-one, three oxysterol species identified in bile.
   Google Scholar
• Yoshida T, Klinkspoor JH, Kuver R et al. Effects of bile salts on cholestan-3b, 5a, 6b-triol-induced apoptosis in dog gallbladder epithelial cells. Biochim. Biophys. Acta 1530, 199–208 (2001).
   Google Scholar
• Kuver R. The expanding universe of bile acid physiology: delving into the mysteries of dark (green) matter. J. Surg. Res. doi:10.1016/j.jss.2012.03.041 (2012) (Epub ahead of print).
   Google Scholar
• Wang YD, Chen WD, Yu D, Forman BM, Huang W. The G-protein-coupled bile acid receptor, Gpbar1 (TGR5), negatively regulates hepatic inflammatory response through antagonizing nuclear factor kappa light-chain enhancer of activated B cells (NF–kB) in mice. Hepatology 54, 1421–1432 (2011).
   Google Scholar
• Fiorucci S, Cipriani S, Mencarelli A, Renga B, Distrutti E, Baldelli F. Counter-regulatory role of bile acid activated receptors in immunity and inflammation. Curr. Mol. Med. 10, 579–595 (2010).
   Google Scholar
• Cipriani S, Mencarelli A, Chini MG, Distrutti E et al. The bile acid receptor Gpbar-1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis. PLoS ONE 6(10), e25637 (2011).
   Google Scholar
• Yoshida T, Klinkspoor JH, Kuver R, Wrenn SP, Kaler EW, Lee SP. Cholestan-3b, 5a, 6b-triol, but not 7-ketocholesterol, suppresses taurocholate-induced mucin secretion by cultured dog gallbladder epithelial cells. FEBS Lett. 478, 113–118 (2000).
   Google Scholar
• Patel T. Increasing incidence and mortality of primary intrahepatic cholangiocarcinoma in the United States. Hepatology 33, 1353–1357 (2001).
   Google Scholar
• Patel T. Cholangiocarcinoma. Nat. Clin. Pract. Gastroenterol. Hepatol. 3, 33–42 (2006).
   Google Scholar
• Smout MJ, Sripa B, Laha T et al. Infection with the carcinogenic human liver fluke, Opisthorchis viverrini. Mol. Biosyst. 7, 1367–1375 (2011).
   Google Scholar
• Yongvanit P, Pinlaor S, Bartsch H. Oxidative and nitrative DNA damage: key events in opisthorchiasis-induced carcinogenesis. Parasitol. Int. 61, 130–135 (2012).
   Google Scholar
• Pinlaor S, Sripa B, Ma N et al. Nitrative and oxidative DNA damage in intrahepatic cholangiocarcinoma patients in relation to tumor invasion. World J. Gastroenterol. 11, 4644–4649 (2005).
   Google Scholar
• Thamavit W, Bhamarapravati N, Saphaphong S, Vajrasthira S, Angsubhakorn S. Effects of dimethylnitrosamine on induction of cholangiocarcinoma in Opisthorchis viverrini-infected Syrian golden hamsters. Cancer Res. 38, 4634–4639 (1978).
   Google Scholar
• Loilome W, Yongvanit P, Wongkham C et al. Altered gene expression in Opisthorchis viverrini-associated cholangiocarcinoma in hamster model. Mol. Carcinog. 45, 279–287 (2006). ▪ Differential display PCR on liver tissues from hamsters induced to develop cholangiocarcinoma identified an oxysterol-binding protein, OSBPL-8, among transcripts that were upregulated compared with control tissue.
   Google Scholar
• Dechakhamphu S, Pinlaor S, Sitthithaworn P, Bartsch H, Yongvanit P. Accumulation of miscoding etheno-DNA adducts and highly expressed DNA repair during liver fluke-induced cholangiocarcinogenesis in hamsters. Mutat. Res. 691, 9–16 (2010).
   Google Scholar
• Dechakhamphu S, Pinlaor S, Sitthithaworn P, Nair J, Bartsch H, Yongvanit P. Lipid peroxidation and etheno DNA adducts in white blood cells of liver fluke-infected patients: protection by plasma alpha-tocopherol and praziquantel. Cancer Epidemiol. Biomarkers Prev. 19, 310–318 (2010).
   Google Scholar
• Loilome W, Wechagama P, Namwat N et al. Expression of oxysterol binding protein isoforms in opisthorchiasis-associated cholangiocarcinoma: a potential molecular marker for tumor metastasis. Parasitol. Int. 61, 136–139 (2012). ▪ In human cholangiocarcinoma tissue, increased levels of OSBPL-7 mRNA and protein were found compared with non-tumor liver tissues. Higher levels of OSBP2 and OSBPL-7 mRNA were found in blood samples from cholangiocarcinoma patients compared with normal controls.
   Google Scholar
• Jusakul A, Loilome W, Namwat N et al. Liver fluke-induced hepatic oxysterols stimulate DNA damage and apoptosis in cultured human cholangiocytes. Mutat. Res. 731, 48–57 (2012). ▪▪ In the hamster model of cholangiocarcinoma induced by Opisthorchis viverrini and NMDA, two oxysterols (cholestan-3b, 5a, 6b-triol and 3-keto-cholesta-4, 6-diene) were found at higher levels in tumor tissues compared with livers from control animals. These two oxysterols were found to induce DNA adduct formation and induce apoptosis in cultured cholangiocytes.
   Google Scholar
• Wehbe H, Henson R, Meng F, Mize-Berge J, Patel T. Interleukin-6 contributes to growth in cholangiocarcinoma cells by aberrant promoter methylation and gene expression. Cancer Res. 66, 10517–10524 (2006).
   Google Scholar
• Yoon JH, Canbay AE, Werneburg NW, Lee SP, Gores GJ. Oxysterols induce cyclooxygenase-2 expression in cholangiocytes: implications for biliary tract carcinogenesis. Hepatology 39, 732–738 (2004).
   Google Scholar
• Jaiswal M, LaRusso NF, Shapiro RA, Billiar TR, Gores GJ. Nitric oxide-mediated inhibition of DNA repair potentiates oxidative DNA damage in cholangiocytes. Gastroenterology 120, 190–199 (2001).
   Google Scholar
• Jaiswal M, LaRusso NF, Burgart LJ, Gores GJ. Inflammatory cytokines induce DNA damage and inhibit DNA repair in cholangiocarcinoma cells by a nitric-oxidedependent mechanism. Cancer Res. 60, 184–190 (2000).
   Google Scholar
• Braconi C, Huang N, Patel T. MicroRNAdependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology 51. 881–890 (2010).
   Google Scholar
• Gallus GN, Dotti MT, Federico A. Clinical and molecular diagnosis of cerebrotendinous xanthomatosis with a review of the mutations in the CYP27A1 gene. Neurol. Sci. 27, 143–149 (2006).
   Google Scholar
• Campbell DJ, Dumur CI, Lamour NF, Dewitt JL, Sirica AE. Novel organotypic culture model of cholangiocarcinoma progression. Hepatol. Res. doi:10.1111/j.1872-034X.01026.x (2012) (Epub ahead of print).
   Google Scholar