Liver fluke-induced hepatic oxysterols stimulate DNA damage and apoptosis in cultured human cholangiocytes

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 731, Issue 1-2, 2012, Pages 48-57

  Jusakul, Apinya ^a   Loilome, Watcharin ^a   Namwat, Nisana ^a   Haigh, W Geoffrey ^c   Kuver, Rahul ^c   Dechakhamphu, Somkid ^a,b   Sukontawarin, Pradit ^a   Pinlaor, Somchai ^a   Lee, Sum P ^d   Yongvanit, Puangrat ^a  

^a KHON KAEN UNIVERSITY   (Thailand)

^b RAJAMANGALA UNIVERSITY OF TECHNOLOGY THANYABURI   (Thailand)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

4 Cholesten 3 one; Apoptosis; Cholangiocarcinoma; Cholestan 3 ,5 ,6 triol; DNA damage; Oxysterol

Indexed keywords

7 KETO CHOLEST 4 ENE; 7 KETO CHOLEST 7 ENE; 7 KETO CHOLESTA 3,5 DIENE; 7 KETO CHOLESTA 4,6 DIENE; CHOLESTANETRIOL; CYTOCHROME C; OXYSTEROL; PROTEIN BAX; PROTEIN BCL 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BILE DUCT CARCINOMA; CARCINOGENESIS; CONTROLLED STUDY; DNA DAMAGE; FASCIOLA HEPATICA; HAMSTER; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; MASS FRAGMENTOGRAPHY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CHOLANGIOCARCINOMA; CHOLESTANOL; CHOLESTENONES; CRICETINAE; DNA DAMAGE; FASCIOLA HEPATICA; FASCIOLIASIS; HUMANS; LIVER; MESOCRICETUS;

CRICETINAE; FASCIOLA HEPATICA; OPISTHORCHIS VIVERRINI;

EID: 84856218714     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2011.10.009     Document Type: Article

References (62)

1. Guardiola F., Codony R., Addis P.B., Rafecas M., Boatella J. Biological effects of oxysterols: current status. Food Chem. Toxicol. 1996, 34:193-211.
2. Smith L.L. Cholesterol autoxidation 1981-1986. Chem. Phys. Lipids 1987, 44:87-125.
3. Russell D.W. Oxysterol biosynthetic enzymes. Biochim. Biophys. Acta 2000, 1529:126-135.
4. Brown A.J., Jessup W. Oxysterols: sources, cellular storage and metabolism, and new insights into their roles in cholesterol homeostasis. Mol. Aspects Med. 2009, 30:111-122.
5. Brown A.J., Jessup W. Oxysterols and atherosclerosis. Atherosclerosis 1999, 142:1-28.
6. Schroepfer G.J. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol. Rev. 2000, 80:361-554.
7. Bjorkhem I. Do oxysterols control cholesterol homeostasis?. J. Clin. Invest. 2002, 110:725-730.
8. Kolsch H., Lutjohann D., von Bergmann K., Heun R. The role of 24S-hydroxycholesterol in Alzheimer's disease. J. Nutr. Health Aging 2003, 7:37-41.
9. Liu H., Yuan L., Xu S., Wang K., Zhang T. Cholestane-3beta,5alpha, 6beta-triol inhibits osteoblastic differentiation and promotes apoptosis of rat bone marrow stromal cells. J. Cell. Biochem. 2005, 96:198-208.
10. Bischoff F. Carcinogenic effects of steroids. Adv. Lipid Res. 1969, 7:165-244.
11. Biasi F., Mascia C., Poli G. The contribution of animal fat oxidation products to colon carcinogenesis, through modulation of TGF-beta1 signaling. Carcinogenesis 2008, 29:890-894.
12. Silva J., Beckedorf A., Bieberich E. Osteoblast-derived oxysterol is a migration-inducing factor for human breast cancer cells. J. Biol. Chem. 2003, 278:25376-25385.
13. Bischoff F. Cocarcinogenic activity of cholesterol oxidation products and sesame oil. J. Natl. Cancer Inst. 1957, 19:977-987.
14. Linseisen J., Wolfram G., Miller A.B. Plasma 7beta-hydroxycholesterol as a possible predictor of lung cancer risk. Cancer Epidemiol. Biomarkers Prev. 2002, 11:1630-1637.
15. Biasi F., Mascia C., Astegiano M., Chiarpotto E., Nano M., Vizio B., Leonarduzzi G., Poli G. Pro-oxidant and proapoptotic effects of cholesterol oxidation products on human colonic epithelial cells: a potential mechanism of inflammatory bowel disease progression. Free Radic. Biol. Med. 2009, 47:1731-1741.
16. Yoon J.H., Canbay A.E., Werneburg N.W., Lee S.P., Gores G.J. Oxysterols induce cyclooxygenase-2 expression in cholangiocytes: implications for biliary tract carcinogenesis. Hepatology 2004, 39:732-738.
17. Jusakul A., Yongvanit P., Loilome W., Namwat N., Kuver R. Mechanisms of oxysterol-induced carcinogenesis. Lipids Health Dis. 2011, 10:44.
18. Cheng Y.W., Kang J.J., Shih Y.L., Lo Y.L., Wang C.F. Cholesterol-3-beta,5-alpha, 6-beta-triol induced genotoxicity through reactive oxygen species formation. Food Chem. Toxicol. 2005, 43:617-622.
19. Gramajo A.L., Zacharias L.C., Neekhra A., Luthra S., Atilano S.R., Chwa M., Brown D.J., Kuppermann B.D., Kenney M.C. Mitochondrial DNA damage induced by 7-ketocholesterol in human retinal pigment epithelial cells in vitro. Invest. Ophthalmol. Vis. Sci. 2010, 51:1164-1170.
20. Lemaire-Ewing S., Prunet C., Montange T., Vejux A., Berthier A., Bessede G., Corcos L., Gambert P., Neel D., Lizard G. Comparison of the cytotoxic, pro-oxidant and pro-inflammatory characteristics of different oxysterols. Cell Biol. Toxicol. 2005, 21:97-114.
21. Lizard G., Gueldry S., Sordet O., Monier S., Athias A., Miguet C., Bessede G., Lemaire S., Solary E., Gambert P. Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production. FASEB J. 1998, 12:1651-1663.
22. Loilome W., Yongvanit P., Wongkham C., Tepsiri N., Sripa B., Sithithaworn P., Hanai S., Miwa M. Altered gene expression in Opisthorchis viverrini-associated cholangiocarcinoma in hamster model. Mol. Carcinog. 2006, 45:279-287.
23. Pinlaor S., Hiraku Y., Ma N., Yongvanit P., Semba R., Oikawa S., Murata M., Sripa B., Sithithaworn P., Kawanishi S. Mechanism of NO-mediated oxidative and nitrative DNA damage in hamsters infected with Opisthorchis viverrini: a model of inflammation-mediated carcinogenesis. Nitric Oxide 2004, 11:175-183.
24. Pinlaor S., Yongvanit P., Hiraku Y., Ma N., Semba R., Oikawa S., Murata M., Sripa B., Sithithaworn P., Kawanishi S. 8-Nitroguanine formation in the liver of hamsters infected with Opisthorchis viverrini. Biochem. Biophys. Res. Commun. 2003, 309:567-571.
25. Yoshida T., Matsuzaki Y., Haigh W.G., Fukushima S., Ikezawa K., Tanaka N., Lee S.P. Origin of oxysterols in hepatic bile of patients with biliary infection. Am. J. Gastroenterol. 2003, 98:2275-2280.
26. Haigh W.G., Wong T., Lee S.P. The production of oxysterols in bile by activated human leukocytes. Biochem. Biophys. Res. Commun. 2006, 343:467-469.
27. 4-etheno-2'-deoxycytidine detected by monoclonal antibodies in lung and liver DNA of rats exposed to vinyl chloride. Carcinogenesis 1989, 10:209-212.
28. 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. 2010, 691:9-16.
29. Sripa B., Kaewkes S. Localisation of parasite antigens and inflammatory responses in experimental opisthorchiasis. Int. J. Parasitol. 2000, 30:735-740.
30. Haigh W.G., Lee S.P. Identification of oxysterols in human bile and pigment gallstones. Gastroenterology 2001, 121:118-123.
31. Namwat N., Amimanan P., Loilome W., Jearanaikoon P., Sripa B., Bhudhisawasdi V., Tassaneeyakul W. Characterization of 5-fluorouracil-resistant cholangiocarcinoma cell lines. Chemotherapy 2008, 54:343-351.
32. Wang Y., Millonig G., Nair J., Patsenker E., Stickel F., Mueller S., Bartsch H., Seitz H.K. Ethanol-induced cytochrome P4502E1 causes carcinogenic etheno-DNA lesions in alcoholic liver disease. Hepatology 2009, 50:453-461.
33. 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. 1978, 38:4634-4639.
34. Pinlaor S., Sripa B., Sithithaworn P., Yongvanit P. Hepatobiliary changes, antibody response, and alteration of liver enzymes in hamsters re-infected with Opisthorchis viverrini. Exp. Parasitol. 2004, 108:32-39.
35. Massey J.B., Pownall H.J. Structures of biologically active oxysterols determine their differential effects on phospholipid membranes. Biochemistry 2006, 45:10747-10758.
36. Olkkonen V.M., Hynynen R. Interactions of oxysterols with membranes and proteins. Mol. Aspects Med. 2009, 30:123-133.
37. Luu B., Moog C. Oxysterols: biological activities and physicochemical studies. Biochimie 1991, 73:1317-1320.
38. Yoshida T., Klinkspoor J.H., Kuver R., Wrenn S.P., Kaler E.W., Lee S.P. Cholestan-3beta,5alpha,6beta-triol, but not 7-ketocholesterol, suppresses taurocholate-induced mucin secretion by cultured dog gallbladder epithelial cells. FEBS Lett. 2000, 478:113-118.
39. Yoshida T., Klinkspoor J.H., Kuver R., Poot M., Rabinovitch P.S., Wrenn S.P., Kaler E.W., Lee S.P. Effects of bile salts on cholestan-3beta, 5alpha, 6beta-triol-induced apoptosis in dog gallbladder epithelial cells. Biochim. Biophys. Acta 2001, 1530:199-208.
40. Jang E.R., Lee C.S. 7-Ketocholesterol induces apoptosis in differentiated PC12 cells via reactive oxygen species-dependent activation of NF-kappaB and Akt pathways. Neurochem. Int. 2011, 58:52-59.
41. Seo D.W., Choi H.S., Lee S.P., Kuver R. Oxysterols from human bile induce apoptosis of canine gallbladder epithelial cells in monolayer culture. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 287:G1247-G1256.
42. O'Callaghan Y.C., Woods J.A., O'Brien N.M. Oxysterol-induced cell death in U937 and HepG2 cells at reduced and normal serum concentrations. Eur. J. Nutr. 1999, 38:255-262.
43. Pinlaor S., Sripa B., Ma N., Hiraku Y., Yongvanit P., Wongkham S., Pairojkul C., Bhudhisawasdi V., Oikawa S., Murata M., Semba R., Kawanishi S. Nitrative and oxidative DNA damage in intrahepatic cholangiocarcinoma patients in relation to tumor invasion. World J. Gastroenterol. 2005, 11:4644-4649.
44. Thanan R., Murata M., Pinlaor S., Sithithaworn P., Khuntikeo N., Tangkanakul W., Hiraku Y., Oikawa S., Yongvanit P., Kawanishi S. Urinary 8-oxo-7,8-dihydro-2'-deoxyguanosine in patients with parasite infection and effect of antiparasitic drug in relation to cholangiocarcinogenesis. Cancer Epidemiol. Biomarkers Prev. 2008, 17:518-524.
45. 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. 2010, 19:310-318.
46. Dechakhamphu S., Yongvanit P., Nair J., Pinlaor S., Sitthithaworn P., Bartsch H. High excretion of etheno adducts in liver fluke-infected patients: protection by praziquantel against DNA damage. Cancer Epidemiol. Biomarkers Prev. 2008, 17:1658-1664.
47. Monier S., Samadi M., Prunet C., Denance M., Laubriet A., Athias A., Berthier A., Steinmetz E., Jurgens G., Negre-Salvayre A., Bessede G., Lemaire-Ewing S., Neel D., Gambert P., Lizard G. Impairment of the cytotoxic and oxidative activities of 7 beta-hydroxycholesterol and 7-ketocholesterol by esterification with oleate. Biochem. Biophys. Res. Commun. 2003, 303:814-824.
48. Liu H., Wang T., Huang K. Cholestane-3beta,5alpha, 6beta-triol-induced reactive oxygen species production promotes mitochondrial dysfunction in isolated mice liver mitochondria. Chem. Biol. Interact. 2009, 179:81-87.
49. Vejux A., Malvitte L., Lizard G. Side effects of oxysterols: cytotoxicity, oxidation, inflammation, and phospholipidosis. Braz. J. Med. Biol. Res. 2008, 41:545-556.
50. 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. 2009, 30:153-170.
51. Pedruzzi E., Guichard C., Ollivier V., Driss F., Fay M., Prunet C., Marie J.C., Pouzet C., Samadi M., Elbim C., O'Dowd Y., Bens M., Vandewalle A., Gougerot-Pocidalo M.A., Lizard G., Ogier-Denis E. NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol. Cell. Biol. 2004, 24:10703-10717.
52. Palozza P., Simone R., Catalano A., Monego G., Barini A., Mele M.C., Parrone N., Trombino S., Picci N., Ranelletti F.O. Lycopene prevention of oxysterol-induced proinflammatory cytokine cascade in human macrophages: inhibition of NF-kappaB nuclear binding and increase in PPARgamma expression. J. Nutr. Biochem. 2011, 22:259-268.
53. Leonarduzzi G., Gamba P., Sottero B., Kadl A., Robbesyn F., Calogero R.A., Biasi F., Chiarpotto E., Leitinger N., Sevanian A., Poli G. Oxysterol-induced up-regulation of MCP-1 expression and synthesis in macrophage cells. Free Radic. Biol. Med. 2005, 39:1152-1161.
54. Jaiswal M., LaRusso N.F., Shapiro R.A., Billiar T.R., Gores G.J. Nitric oxide-mediated inhibition of DNA repair potentiates oxidative DNA damage in cholangiocytes. Gastroenterology 2001, 120:190-199.
55. Jaiswal M., LaRusso N.F., Burgart L.J., Gores G.J. Inflammatory cytokines induce DNA damage and inhibit DNA repair in cholangiocarcinoma cells by a nitric oxide-dependent mechanism. Cancer Res. 2000, 60:184-190.
56. Jones L.E., Ying L., Hofseth A.B., Jelezcova E., Sobol R.W., Ambs S., Harris C.C., Espey M.G., Hofseth L.J., Wyatt M.D. Differential effects of reactive nitrogen species on DNA base excision repair initiated by the alkyladenine DNA glycosylase. Carcinogenesis 2009, 30:2123-2129.
57. Bernstein H., Bernstein C., Payne C.M., Dvorakova K., Garewal H. Bile acids as carcinogens in human gastrointestinal cancers. Mutat. Res. 2005, 589:47-65.
58. Crowley-Weber C.L., Payne C.M., Gleason-Guzman M., Watts G.S., Futscher B., Waltmire C.N., Crowley C., Dvorakova K., Bernstein C., Craven M., Garewal H., Bernstein H. Development and molecular characterization of HCT-116 cell lines resistant to the tumor promoter and multiple stress-inducer, deoxycholate. Carcinogenesis 2002, 23:2063-2080.
59. Magnuson B.A., Shirtliff N., Bird R.P. Resistance of aberrant crypt foci to apoptosis induced by azoxymethane in rats chronically fed cholic acid. Carcinogenesis 1994, 15:1459-1462.
60. Yongvanit P., Pinlaor S., Bartsch H. Oxidative and nitrative DNA damage: key events in opisthorchiasis-induced carcinogenesis. Parasitol. Int. 2011, doi:10.1016/j.parint.2011.06.011.
61. Prakobwong S., Yongvanit P., Hiraku Y., Pairojkul C., Sithithaworn P., Pinlaor P., Pinlaor S. Involvement of MMP-9 in peribiliary fibrosis and cholangiocarcinogenesis via Rac1-dependent DNA damage in a hamster model. Int. J. Cancer 2010, 127:2576-2587.
62. Prakobwong S., Pinlaor S., Yongvanit P., Sithithaworn P., Pairojkul C., Hiraku Y. Time profiles of the expression of metalloproteinases, tissue inhibitors of metalloproteases, cytokines and collagens in hamsters infected with Opisthorchis viverrini with special reference to peribiliary fibrosis and liver injury. Int. J. Parasitol. 2009, 39:825-835.