Ursodeoxycholic acid decreases bilirubin-induced osteoblast apoptosis

European Journal of Clinical Investigation

Volumn 44, Issue 12, 2014, Pages 1206-1214

  Ruiz Gaspà, Silvia ^a   Dubreuil, Marta ^a   Guañabens, Nuria ^a   Combalia, Andrés ^a   Peris, Pilar ^a   Monegal, Ana ^a   Parés, Albert ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Bile acids; Bone turnover; Cholestasis; Osteoporosis; Primary biliary cirrhosis

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIOXIDANT; BILIRUBIN; CAMPTOTHECIN; CHOLAGOGUE; DETERGENT; LITHOCHOLIC ACID; PROTEIN BAX; URSODEOXYCHOLIC ACID;

APOPTOSIS; DRUG EFFECTS; GENETICS; HUMAN; OSTEOBLAST; TUMOR CELL LINE; UPREGULATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTIOXIDANTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BILIRUBIN; CAMPTOTHECIN; CELL LINE, TUMOR; CHOLAGOGUES AND CHOLERETICS; DETERGENTS; HUMANS; LITHOCHOLIC ACID; OSTEOBLASTS; UP-REGULATION; URSODEOXYCHOLIC ACID;

EID: 84912059622     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/eci.12355     Document Type: Article

References (45)

1. Guañabens N, Parés A, Mariñoso L, Brancós MA, Piera C, Serrano S et al. Factors influencing the development of metabolic bone disease in primary biliary cirrhosis. Am J Gastroentero 1990;85:1356-62.
2. Eastell R, Dickson ER, Hodgson SF, Wiesner RH, Porayko MK, Wahner HW et al. Rates of vertebral bone loss before and after liver transplantation in women with primary biliary cirrhosis. Hepatology 1991;14:296-300.
3. Menon KV, Angulo P, Weston S, Dickson ER, Lindor KD. Bone disease in primary biliary cirrhosis: independent indicators and rate of progression. Hepatology 2001;35:316-23.
4. Guañabens N, Parés A, Ros I, Caballería L, Pons F, Vidal S et al. Severity of cholestasis and advanced histological stage but not menopausal status are the major risk factors for osteoporosis in primary biliary cirrhosis. J Hepatol 2005;42:573-7.
5. Janes CH, Dickson ER, Okazaki R, Bonde S, McDonagh AF, Riggs BL. Role of hyperbilirubinemia in the impairment of osteoblast proliferation associated with cholestatic jaundice. J Clin Invest 1995;95:2581-6.
6. Ruiz-Gaspà S, Martinez-Ferrer A, Guañabens N, Dubreuil M, Peris P, Enjuanes A et al. Effects of bilirubin and sera from jaundiced patients on osteoblasts: contribution to the development of osteoporosis in liver diseases. Hepatology 2011;54:2104-13.
7. Dubreuil M, Ruiz-Gaspà S, Guañabens N, Peris P, Alvarez L, Monegal A et al. Ursodeoxycholic acid increases differentiation and mineralization and neutralizes the damaging effects of bilirubin on osteoblastic cells. Liver Int 2013;33:1029-38.
8. Ruiz-Gaspà S, Guañabens N, Enjuanes A, Peris P, Martinez-Ferrer A, de Osaba MJ et al. Lithocholic acid downregulates vitamin D effects in human osteoblasts. Eur J Clin Invest 2010;40:25-34.
9. Lee YM, Kaplan MM. The natural history of PBC: has it changed? Semin Liver Dis 2005;25:321-6.
10. Parés A, Caballeria L, Rodés J. Excellent long-term survival in patients with primary biliary cirrhosis and biochemical response to ursodeoxycholic acid. Gastroenterology 2006;130:715-20.
11. Beuers U, Boberg KM, Chapman RW, Chazouillères O, Invernizzi P, Jones DEJ et al. EASL clinical practice guidelines: management of cholestatic liver diseases. J Hepatol 2009;51:237-67.
12. Paumgartner G, Beuers U. Ursodeoxycholic acid in cholestatic liver disease: mechanisms of action and therapeutic use revisited. Hepatology 2002;36:525-31.
13. Lindor KD, Janes CH, Crippin JS, Jorgensen RA, Dickson ER. Bone disease in primary biliary cirrhosis: does ursodeoxycholic acid make a difference? Hepatology 1995;21:389-92.
14. Benz C, Angermüller S, Töx U, Klöters-Plachky P, Riedel HD, Sauer P et al. Effect of tauroursodeoxycholic acid on bile acid-induced apoptosis and cytolysis in rat hepatocytes. J Hepatol 1998;28:99-106.
15. Qiao L, Yacoub A, Studer E, Gupta S, Pei XY, Grant S et al. Inhibition of the mitogen activated protein kinase (MAPK) and phosphatidyl inositol 3-kinase (PI3K) pathways enhances ursodeoxycholic acid-induced apoptosis in primary rodent hepatocytes. Hepatology 2002;35:779-89.
16. Im E, Martinez JD. Ursodeoxycholic acid (UDCA) can inhibit deoxycholic acid (DCA)-induced apoptosis via modulation of EGFR/Raf-1/ERK signaling in human colon cancer cells. J Nutr 2004;134:483-6.
17. Castro RE, Solá S, Ramalho RM, Steer CJ, Rodrigues CM. The bile acid tauroursodeoxycholic acid modulates phosphorylation and translocation of bad via phosphatidylinositol 3-kinase in glutamate-induced apoptosis of rat cortical neurons. J Pharmacol Exp Ther 2004;311:845-52.
18. Rajesh KG, Suzuki R, Maeda H, Yamamoto M, Yutong X, Sasaguri S. Hydrophilic bile salt ursodeoxycholic acid protects myocardium against reperfusion injury in a PI3K/Akt dependent pathway. J Mol Cell Cardiol 2005;39:766-76.
19. Robey PG, Termine JD. Human bone cells in vitro. Calcif Tissue Int 1985;37:453-60.
20. Hernández MV, Guañabens N, Alvarez L, Monegal A, Peris P, Riba J et al. Immunocytochemical evidence on the effects of glucocorticoids on type I collagen synthesis in human osteoblastic cells. Calcif Tissue Int 2004;74:284-93.
21. Lezcano V, Bellido T, Plotkin LI, Boland R, Morelli S. Role of connexin 43 in the mechanism of action of alendronate: dissociation of anti-apoptotic and proliferative signaling pathways. Arch Biochem Biophys 2012;518:95-102.
22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)). Methods 2001;25:402-8.
23. Raisz LG. Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J Clin Invest 2005;115:3318-25.
24. Jilka RL, Weinstein RS, Bellido T, Parfitt AM, Manolagas SC. Osteoblast programmed cell death (apoptosis): modulation by growth factors and cytokines. J Bone Miner Res 1998;13:793-802.
25. Jilka RL, Weinstein RS, Parfitt AM, Manolagas SC. Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. J Bone Miner Res 2007;22:1492-501.
26. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 1997;3:614-20.
27. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998;281:1322-6.
28. Kozoni V, Tsioulias G, Shiff S, Rigas B. The effect of lithocholic acid on proliferation and apoptosis during the early stages of colon carcinogenesis: differential effect on apoptosis in the presence of a colon carcinogen. Carcinogenesis 2000;21:999-1005.
29. Katona BW, Anant S, Covey DF, Stenson WF. Characterization of enantiomeric bile acid-induced apoptosis in colon cancer cell lines. J Biol Chem 2009;284:3354-64.
30. Rodrigues CM, Solá S, Brites D. Bilirubin induces apoptosis via the mitochondrial pathway in developing rat brain neurons. Hepatology 2002;35:1186-95.
31. Grojean S, Koziel V, Vert P, Daval JL. Bilirubin induces apoptosis via activation of NMDA receptors in developing rat brain neurons. Exp Neurol 2000;166:334-41.
32. Silva RF, Rodrigues CM, Brites D. Bilirubin-induced apoptosis in cultured rat neural cells is aggravated by chenodeoxycholic acid but prevented by ursodeoxycholic acid. J Hepatol 2001;34:402-8.
33. Rodrigues CM, Steer CJ. The therapeutic effects of ursodeoxycholic acid as an anti-apoptotic agent. Expert Opin Investig Drugs 2001;10:1243-53.
34. Amaral JD, Castro RE, Solá S, Steer CJ, Rodrigues CM. p53 is a key molecular target of ursodeoxycholic acid in regulating apoptosis. J Biol Chem 2007;282:34250-9.
35. Castro RE, Solá S, Ma X, Ramalho RM, Kren BT, Steer CJ et al. A distinct microarray gene expression profile in primary rat hepatocytes incubated with ursodeoxycholic acid. J Hepatol 2005;42:897-906.
36. Castro RE, Amaral JD, Solá S, Kren BT, Steer CJ, Rodrigues CM. Differential regulation of cyclin D1 and cell death by bile acids in primary rat hepatocytes. Am J Physiol Gastrointest Liver Physiol 2007;293:G327-34.
37. Pusl T, Vennegeerts T, Wimmer R, Denk GU, Beuers U, Rust C. Tauroursodeoxycholic acid reduces bile acid-induced apoptosis by modulation of AP-1. Biochem Biophys Res Commun 2008;367:208-12.
38. Tsagarakis NJ, Drygiannakis I, Batistakis AG, Kolios G, Kouroumalis EA. A concentration-dependent effect of ursodeoxycholate on apoptosis and caspases activities of HepG2 hepatocellular carcinoma cells. Eur J Pharmacol 2010;640:1-7.
39. Liu H, Qin CY, Han GQ, Xu HW, Meng M, Yang Z. Mechanism of apoptotic effects induced selectively by ursodeoxycholic acid on human hepatoma cell lines. World J Gastroenterol 2007;13:1652-8.
40. Rodrigues CM, Fan G, Ma X, Kren BT, Steer CJ. A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 1998;101:2790-9.
41. Solá S, Amaral JD, Aranha MM, Steer CJ, Rodrigues CM. Modulation of hepatocyte apoptosis: cross-talk between bile acids and nuclear steroid receptors. Curr Med Chem 2006;13:3039-51.
42. Ramalho RM, Viana RJ, Low WC, Steer CJ, Rodrigues CM. Bile acids and apoptosis modulation: an emerging role in experimental Alzheimer's disease. Trends Mol Med 2008;14:54-62.
43. Reed JC. Apoptosis-based therapies. Nat Rev Drug Discov 2002;1:111-21.
44. Verma A, Maxwell JD, Ang L, Davis T, Hodges S, Northfield TC et al. Ursodeoxycholic acid enhances fractional calcium absorption in primary biliary cirrhosis. Osteoporos Int 2002;13:677-82.
45. Guañabens N, Cerdá D, Monegal A, Pons F, Caballería L, Peris P. Low bone mass and severity of cholestasis affect fracture risk in patients with primary biliary cirrhosis. Gastroenterology 2010;138:2348-56.