MOLECULAR MECHANISMS THAT LEAD TO CHOLANGIOCARCINOMA, DURING CHRONIC INFECTION OF LIVER FLUKES
Abstract
Cholangiocarcinoma is a malignant tumor, characterized by poor prognosis and a low five-year survival rate. There is a clear correlation between the incidence of opisthorchiasis and high incidence of cholangiocarcinoma in South-East Asia. Liver flukes Clonorchis sinensis and Opisthorchis viverrini are I class carcinogens. There are some endemic regions of opisthorchiasis In the Russian Federation. The most important factor that leads to carcinogenesis during liver fluke infection is chronic inflammation. This review article focuses on the communication of chronic inflammation caused by invasion of liver flukes and cholangiocarcinoma. This paper summarizes the current knowledge about the risk factors for cholangiocarcinoma, as well as knowledge about the molecular aspects of the induction of carcinogenesis by liver flukes.
About the Authors
A. O. BogdanovRussian Federation
Bogdanov Alexandr Olegovich, student, Medical-Biological Faculty.
E-mail: AxeBogdanov@gmail.com. SPIN-code: 7566-5860.
D. V. Prokudina
Russian Federation
Prokudina Daria Vladimirovna, student, Medical-Biological Faculty.
E-mail: dariya1992@mail.ru. SPIN-code: 7768-5902.
A. N. Baykov
Russian Federation
Baikov Alexandr Nikolaevich, MD, DSc, Head of Central Research Laboratory.
SPIN-code: 3510-4400.
I. V. Saltykova
Russian Federation
Saltykova Irina Vladimirovna, MD, PhD, Researcher, Central Research Laboratory.
E-mail: ira.saltikova@mail.ru. SPIN-code: 9432-3873.
References
1. The official website of the World Health Organization (URL: http://www.who.int 25.04.2015)
2. The official website of Rospotrebnadzor (URL: http://77.rospotrebnadzor.ru 30.04.2015)
3. The official website of European Society for Medical Oncology(URL: http://www.esmo.org 27.06.2015)
4. Bazin I.S., Garin A.M. Treatment of cholangiocellular bile ductcancer, gallbladder cancer and cancer of the papilla of Vater // Russkij medicinskij zhurnal. 2002. № 24. P. 1103–1108. [in Russian]
5. Brazhnikova N.A., Tolkaeva M.V. Cancer of liver, biliary tracts and pancreas at chronic opisthorchosis // Bjulleten’ sibirskoj mediciny. 2002. № 2. P. 71–77. [in Russian]
6. Klisho E.V., Kondakova I.V., Choinzonov E.L., Shishkin D.A., Cheremisina O.V., Chizhevskaya S.Yu. Role of MMP-2 and MMP-9 in the development and prognosis of squamous cell head and neck carcinoma // Sibirskij onkologicheskij zhurnal. 2009. № 6. P. 48–53. [in Russian]
7. Starinskij V.V., Kaprin A.D., Petrova G.V. Malignancies in Russia in 2013 (morbidity and mortality). M., 2015. P. 4–8. [in Russian]
8. Braconi C., Patel T. Cholangiocarcinoma: new insights into disease pathogenesis and biology // Infect. Dis. Clin. North. Am. 2010. Vol. 24 (4). P. 871–884. doi: 10.1016/j.idc.2010.07.006.
9. Cardinale V., Wang Y., Carpino G., Reid L.M., Gaudio E., Alvaro D. Mucin-producing cholangiocarcinoma might derive from biliary tree stem/ progenitor cells located in peribiliary glands // Hepatology. 2012. Vol. 55 (6). P. 2041–2042. doi: 10.1002/hep.25587.
10. Choi B.I., Han J.K., Hong S.T., Lee K.H. Clonorchiasis and cholangiocarcinoma: etiologic relationship and imaging diagnosis // Clin. Microbiol. Rev. 2004. Vol. 17 (3). P. 540–552.
11. Chen Y.J., Luo J., Yang G.Y., Yang K., Wen S.Q., Zou S.Q. Mutual regulation between microRNA-373 and methyl-CpG-binding domain protein 2 in hilar cholangiocarcinoma // World J. Gastroenterol. 2012. Vol. 18 (29). P. 3849–3861. doi: 10.3748/wjg.v18.i29.3849.
12. Deenonpoe R., Chomvarin C., Pairojkul C., Chamgramol Y., Loukas A., Brindley P.J., Sripa B. The Carcinogenic Liver Fluke Opisthorchis viverrini is a Reservoir for Species of Helicobacter // Asian Pac. J. Cancer Prev. 2015. Vol. 16 (5). P. 1751–1758.
13. 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. Vol. 19 (1). P. 310–318. doi: 10.1158/1055-9965.EPI-09-0849.
14. Fukase K., Ohtsuka H., Onogawa T., Oshio H., Ii T., Mutoh M., Katayose Y., Rikiyama T., Oikawa M., Motoi F., Egawa S., Abe T., Unno M. Bile acids repress E-cadherin through the induction of Snail and increase cancer invasiveness in human hepatobiliary carcinoma // Cancer Sci. 2008. Vol. 99 (9). P. 1785–1792. doi: 10.1111/j.1349-7006.2008.00898.x.
15. Hirashita T., Iwashita Y., Ohta M., Komori Y., Eguchi H., Yada K., Kitano S. Expression of Matrix Metalloproteinase-7 is an Unfavorable Prognostic Factor in Intrahepatic Cholangiocarcinoma // J. Gastrointest. Surg. 2012. Vol. 16 (4). P. 842–848. doi: 10.1007/s11605-011-1813-2.
16. Hirata K., Takada M., Suzuki Y., Kuroda Y. Expression of receptor for advanced glycation end products (RAGE) in human biliary cancer cells // Hepatogastroenterology. 2003. Vol. 50 (53). P. 1200–1207.
17. Hoffmann S., Friedrichs U., Eichler W., Rosenthal A., Wiedemann P. Advanced glycation end products induce choroidal endothelial cell proliferation, matrix metalloproteinase-2 and VEGF upregulation in vitro // Graefes Arch. Clin. Exp. Ophthalmol. 2002. Vol. 240 (12). P. 996–1002.
18. Isomoto H., Kobayashi S., Werneburg N.W., Bronk S.F., Guicciardi M.E., Frank D.A., Gores G.J. Interleukin 6 upregulates myeloid cell leukemia-1 expression through a STAT3 pathway in cholangiocarcinoma cells // Hepatology. 2005. Vol. 42 (6). P. 1329–1338.
19. Jing H., Lee S. NF-κB in cellular senescence and cancer treatment // Mol. Cells. 2014. Vol. 37 (3). P. 189–195. doi: 10.14348/molcells.2014.2353.
20. Jusakul A., Loilome W., Namwat N., Haigh W.G., Kuver R., Dechakhamphu S., Sukontawarin P., Pinlaor S., Lee S.P., Yongvanit P. Liver fluke-induced hepatic oxysterols stimulate DNA damage and apoptosis in cultured human cholangiocytes // Mutat. Res. 2012. Vol. 731 (1–2). P. 48–57. doi: 10.1016/j.mrfmmm.2011.10.009.
21. Jusakul A., Yongvanit P., Loilome W., Namwat N., Kuver R. Mechanisms of oxysterol-induced carcinogenesis // Lipids Health Dis. 2011. Vol. 10. P. 1–8. doi: 10.1186/1476-511X-10-44.
22. Kaewpitoon N., Kaewpitoon S.J., Pengsaa P., Sripa B. Opisthorchis viverrini: the carcinogenic human liver fluke // World J. Gastroenterol. 2008. Vol. 14 (5). P. 666–674.
23. Komori J., Marusawa H., Machimoto T., Endo Y., Kinoshita K., Kou T., Haga H., Ikai I., Uemoto S., Chiba T. Activation-induced cytidine deaminase links bile duct inflammation to human cholangiocarcinoma // Hepatology. 2008. Vol. 47 (3). P. 888–896. doi: 10.1002/hep.22125.
24. Li B., Han Q., Zhu Y., Yu Y., Wang J., Jiang X. Down-regulation of miR-214 contributes to intrahepatic cholangiocarcinoma metastasis by targeting Twist // FEBS J. 2012. Vol. 79 (13). P. 2393–2398. doi: 10.1111/j.1742-4658.2012.08618.x.
25. 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. Vol. 12 (15). P. 1651–1663.
26. Losada H., Hirsch M., Guzmán P., Fonseca F., Hofmann E., Alanís M. Fascioliasis simulating an intrahepatic cholangiocarcinoma-Case report with imaging and pathology correlation // Hepatobiliary Surg. Nutr. 2015. Vol. 4 (1). E. 1–7. doi: 10.3978/j.issn.2304-3881.2014.09.15.
27. Maksimova G.A., Zhukova N.A., Kashina E.V., Lvova M.N., Katokhin A.V., Tolstikova T.G., Mordvinov V.A. Role of opisthorchis felineus on induction of bile duct cancer // Parazitologiia. 2015. Vol. 49 (1). P. 3–11.
28. Mathema V.B., Na-Bangchang K. Current insights on cholangiocarcinoma research: a brief review // Asian Pac. J. Cancer Prev. 2015. Vol. 16 (4). P. 1307–1313.
29. Ninlawan K., O’Hara S.P., Splinter P.L., Yongvanit P., Kaewkes S., Surapaitoon A., LaRusso N.F., Sripa B. Opisthorchis viverrini excretory/ secretory products induce toll-like receptor 4 upregulation and production of interleukin 6 and 8 in cholangiocyte // Parasitol. Int. 2010. Vol. 59 (4). P.616–621. doi: 10.1016/j.parint.2010.09.008.
30. Pal S., Bhattacharjee A., Ali A., Mandal N.C., Mandal S.C., Pal M. Chronic inflammation and cancer: potential chemoprevention through nuclear factor kappa B and p53 mutual antagonism // J. Inflamm. (Lond). 2014. Vol. 11. P. 1–28. doi: 10.1186/1476-9255-11-23. eCollection 2014.
31. Patel T. Cholangiocarcinoma // Nat. Clin. Pract. Gastroenterol. Hepatol. 2006. Vol. 3 (1). P. 33–42.
32. Pinlaor S., Hiraku Y., Ma N., Yongvanit P., Semba R., Oikawa S., Murata M., Sripa B., Sithithaworn P., Kawanishi S. Mechanism of NOmediated oxidative and nitrative DNA damage in hamsters infected with Opisthorchis viverrini: a model of inflammation-mediated carcinogenesis // Nitric Oxide. 2004. Vol. 11 (2). P. 175–183.
33. Pinlaor S., Hiraku Y., Yongvanit P., Tada-Oikawa S., Ma N., Pinlaor P., Sithithaworn P., Sripa B., Murata M., Oikawa S., Kawanishi S. iNOSdependent DNA damage via NF-kappaB expression in hamsters infected with Opisthorchis viverrini and its suppression by the antihelminthic drug praziquantel // Int. J. Cancer. 2006. Vol. 119 (5). P. 1067–1072.
34. Pinlaor S., Ma N., Hiraku Y., Yongvanit P., Semba R., Oikawa S., Murata M., Sripa B., Sithithaworn P., Kawanishi S. Repeated infection with Opisthorchis viverrini induces accumulation of 8-nitroguanine and 8-oxo- 7,8-dihydro-20-deoxyguanine in the bile duct of hamsters via inducible nitric oxide synthase // Carcinogenesis. 2004. Vol. 25 (8). P. 1535–1542.
35. Smout M.J., Laha T., Mulvenna J., Sripa B., Suttiprapa S., Jones A., Brindley P.J., Loukas A. A Granulin-Like Growth Factor Secreted by the Carcinogenic Liver Fluke, Opisthorchis viverrini, Promotes Proliferation of Host Cells // PLoS Pathogens. 2009. Vol. 5 (10). P. 3–13. doi: 10.1371/journal.ppat.1000611.
36. Spirlì C., Fabris L., Duner E., Fiorotto R., Ballardini G., Roskams T., Larusso N.F., Sonzogni A., Okolicsanyi L., Strazzabosco M. Cytokinestimulated nitric oxide production inhibits adenylyl cyclase and cAMPdependent secretion in cholangiocytes // Gastroenterology. 2003. Vol. 124 (3). P. 737–753.
37. Sripa B., Brindley P.J., Mulvenna J., Laha T., Smout M.J., Mairiang E., Bethony J.M., Loukas A. The tumorigenic liver fluke Opisthorchis viverrini - multiple pathways to cancer // Trends Parasitol. 2012. Vol. 28 (10). P. 395–407. doi: 10.1016/j.pt.2012.07.006.
38. Sripa B., Kaewkes S., Sithithaworn P., Mairiang E., Laha T., Smout M., Pairojkul C., Bhudhisawasdi V., Tesana S., Thinkamrop B., Bethony J.M., Loukas A., Brindley P.J. Liver Fluke Induces Cholangiocarcinoma // PLoS Medicine. 2007. Vol. 4 (7). P. 1148–1155.
39. Sripa B., Thinkhamrop B., Mairiang E., Laha T., Kaewkes S., Sithithaworn P., Periago M.V., Bhudhisawasdi V., Yonglitthipagon P., Mulvenna J., Brindley P.J., Loukas A., Bethony J.M. Elevated plasma IL-6 associates with increased risk of advanced fibrosis and cholangiocarcinoma in individuals infected by Opisthorchis viverrini // PLoS Negl. Trop. Dis. 2012. Vol. 6 (5). P. 1–9. doi: 10.1371/journal.pntd.0001654.
40. Sripa J., Laha T., To J., Brindley P.J., Sripa B., Kaewkes S., Dalton J.P., Robinson M.W. Secreted cysteine proteases of the carcinogenic liver fluke, Opisthorchis viverrini: regulation of cathepsin F activation by autocatalysis and trans-processing by cathepsin B // Cell Microbiol. 2010. Vol. 12 (6). P. 781–795. doi: 10.1111/j.1462-5822.2010.01433.x.
41. Sugawara H., Yasoshima M., Katayanagi K., Kono N., Watanabe Y., Harada K., Nakanuma Y. Relationship between interleukin-6 and proliferation and differentiation in cholangiocarcinoma // Histopathology. 1998. Vol. 33 (2). P. 145–153.
42. Tielens A.G., van den Heuvel J.M., van den Bergh S.G. The energy metabolism of Fasciola hepatica during its development in the final host // Mol. Biochem. Parasitol. 1984. Vol. 13 (3). P. 301–307.
43. Tyson G.L., El-Serag H.B. Risk factors for cholangiocarcinoma // Hepatology. 2011. Vol. 54 (1). P. 173–184. doi: 10.1002/hep.24351.
44. Wang L.J., He C.C., Sui X., Cai M.J., Zhou C.Y., Ma J.L., Wu L., Wang H., Han S.X., Zhu Q. MiR-21 promotes intrahepatic cholangiocarcinoma proliferation and growth in vitro and in vivo by targeting PTPN14 and PTEN // Oncotarget. 2015. Vol. 6 (8). P. 5932–5946.
45. 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. 2006. Vol. 66 (21). P. 10517–10524.
46. Werneburg N.W., Yoon J.H., Higuchi H., Gores G.J. Bile acids activate EGF receptor via a TGF-alpha-dependent mechanism in human cholangiocyte cell lines // Am. J. Physiol. Gastrointest. Liver Physiol. 2003. Vol. 285 (1). P. 31–36.
47. Wonkchalee O., Boonmars T., Kaewkes S., Chamgramol Y., Pairojkul C., Wu Z., Juasook A., Sudsarn P., Boonjaraspinyo S. Opisthorchis viverrini infection causes liver and biliary cirrhosis in gerbils // Parasitol. Res. 2011. Vol. 109 (3). P. 545–551. doi: 10.1007/s00436-011-2282-y.
48. Yoon J.H., Werneburg N.W., Higuchi H., Canbay A.E., Kaufmann S.H., Akgul C., Edwards S.W., Gores G.J. Bile acids inhibit Mcl-1 protein turnover via an epidermal growth factor receptor/Raf-1-dependent mechanism // Cancer Res. 2002. Vol. 62 (22). P. 6500–6505.
49. Yu Q., Stamenkovic I. Cell surface-localized matrix metalloproteinase- 9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis // Genes Dev. 2000. Vol. 14 (2). P. 163–176.
50. Zhou D., Wang J.D., Weng M.Z., Zhang Y., Wang X.F., Gong W., Quan Z.W. Infections of Helicobacter spp. in the biliary system are associated with biliary tract cancer: a meta-analysis // Eur. J. Gastroenterol. Hepatol. 2013. Vol. 25 (4). P. 447–454. doi: 10.1097/MEG.0b013e32835c0362.
Review
For citations:
Bogdanov A.O., Prokudina D.V., Baykov A.N., Saltykova I.V. MOLECULAR MECHANISMS THAT LEAD TO CHOLANGIOCARCINOMA, DURING CHRONIC INFECTION OF LIVER FLUKES. Siberian journal of oncology. 2015;(6):83-90. (In Russ.)