The characteristics of the expression of heat shock proteins and cox-2 in the liver of hamsters infected with Clonorchis sinensis, and the change of endocrine hormones and cytokines (original) (raw)
Folia Parasitologica 59[4] 255-263 (2012) | DOI: 10.14411/fp.2012.036
Department of Medical Zoology, Kyung Hee University School of Medicine, 26 Kyunghee-daero, Dongdaemun-gu, Seoul 130-701, Republic of Korea
The liver fluke Clonorchis sinensis (Digenea) is a high-risk parasite that causes serious diseases such as cirrhosis, carcinogenic liver damage and clonorchiasis in East Asia. This study was conducted to evaluate the relationship between stress/endocrine hormones and inflammation induced by infection as well as the expression of heat shock proteins (hsp-27, hsp-90), cox-2 and cytokines in the livers of hamsters infected with C. sinensis. The average body weight of infected hamsters decreased up to 25% compared with that of the control group, and bile duct hyperplasia with inflammation, liver fibrosis and hepatic necrosis were observed in _C. sinensis_-infected livers. The expression of hsp-27, hsp-90, and cox-2 was significantly increased in the livers of _C. sinensis_-infected hamsters compared with the control group. Moreover, the expression levels of inflammatory cytokines (IL-1β, IL-2, TGF-β2 and IFN-α1) were markedly increased in the livers of the infected group compared with those of the control group. Consistently, plasma IL-3 and IL-6 levels gradually increased during the infection period, and the concentration levels of testosterone, luteinizing hormone (LH), follicle-stimulating hormone (FSH), corticosterone, and adrenocorticotropic hormone (ACTH) in _C. sinensis_-infected hamsters increased over 25%, compared with those of the uninfected normal group. These results demonstrate that C. sinensis infection may increase the expression of hsp27, hsp90 and cox-2 as well as it may cause periductal fibrosis, chronic inflammation and hepatic necrosis in the liver. Furthermore, the results indicate that C. sinensis infection induces not only stress-induced hormone imbalance but also the sustained secretion of inflammatory cytokines through chronic stress/stimuli.
Keywords: liver fluke, Digenea, cytokines, cox-2, heat shock proteins, inflammation
Received: January 9, 2012; Accepted: August 14, 2012; Published: December 1, 2012 Show citation
- BibTeX (.bib)
- Bookends (.ris)
- EasyBib (.ris)
- EndNote (.enw)
- EndNote 8 (.xml)
- ISI WoS (.isi)
- Medlars (.medlars)
- Mendeley (.ris)
- MODS (.xml)
- Papers (.ris)
- RefWorks (.txt)
- RefManager (.ris)
- RIS (.ris)
- MS Word (.xml)
- Zotero (.ris)
References
- Alves O liveira L.F., Moreno E.C., Gazzinelli G., Martins Filho O.A., Silveira A.M., Gazzinelli A., Malaquias L.C., LoVerde P., Leite P.M., Correa-Oliveira R. 2006: Cytokine production associated with periportal fibrosis during chronic schistosomiasis mansoni in humans. Infect. Immun. 74: 1215-1221
Go to original source...
Go to PubMed... - Bekisz J., Schmeisser H., Hernandez J., Goldman N.D., Zoon K.C. 2004: Human interferons alpha, beta and omega. Growth Factors 22: 243-251
Go to original source...
Go to PubMed... - Benjamin I.J., McMillan D.R. 1998: Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ. Res. 83: 117-132
Go to original source...
Go to PubMed... - Berezowski P., Strzalka-Mrozik B., Forminska-Kapuscik M., Mazurek U., Filipek E., Nawrocka L., Pieczara E., Banasiak P., Kimsa M. 2012: Posttraumatic temporal TGF-β mRNA expression in lens epithelial cells of paediatric patients. Folia. Biol. 58: 24-29
- Borges J.C., Ramos C.H. 2005: Protein folding assisted by chaperones. Protein. Pept. Lett. 12: 257-261.
Go to original source...
Go to PubMed... - Bouvard V., Baan R., Straif K., Grosse Y., Secretan B., El Ghissassi F., Benbrahim -Tallaa L., Guha N, Freeman C., Galichet L., Cogliano V. 2009: WHO International Agency for Research on Cancer Monograph Working Group. A review of human carcinogens-Part B: biological agents. Lancet Oncol. 10: 321-322
Go to original source...
Go to PubMed... - Caraty A., Miller D.W., Delaleu B., Martin G.B. 1997: Stimulation of LH secretion in sheep by central administration of corticotrophin-releasing hormone. J. Reprod. Fertil. 111: 249-257
Go to original source...
Go to PubMed... - Chandrashekar V., Majumdar S.S., Bartke A. 1994: Assessment of the role of follicle-stimulating hormone and prolactin in the control of testicular endocrine function in adult djungarian hamsters (Phodopus sungorus) exposed to either short or long photoperiod. Biol. Reprod. 50: 82-87
Go to original source...
Go to PubMed... - Cho S.H., Lee K.Y., Lee B.C., Cho P.Y., Cheun H.I., Hong S.T., Sohn W.M., Kim T.S. 2008: Prevalence of clonorchiasis in southern endemic areas of Korea in 2006. Korean J. Parasitol. 46: 133-137
Go to original source...
Go to PubMed... - Choi W.H., Chu J.P., Jiang M., Lee Y.S., Kim B.S., Kim D.G., Park Y.K. 2010: Analysis of parasitic diseases diagnosed by tissue biopsy specimens at KyungHee Medical Center (1984- 2005) in Seoul, Korea. Kor. J. Parasitol. 48: 85-88
Go to original source...
Go to PubMed... - Choi W.H., Jiang M.H., Chu J.P. 2012: Antiparasitic effects of Zingiber officinale (ginger) extract against Toxoplasma gondii. J. Appl. Biomed. In press. DOI: 10.2478/v10136-012-0014-y
Go to original source... - Choi Y.K., Yoon B.I., Won Y.S., Lee C.H., Hyun B.H., Kim H.C., Oh G.T., Kim D.Y. 2003: Cytokine responses in mice infected with Clonorchis sinensis. Parasitol. Res. 91: 87-93
Go to original source...
Go to PubMed... - Coussens L.M., Werb Z. 2002: Inflammation and cancer. Nature 420: 860-867
Go to original source...
Go to PubMed... - Dikic D., Budec M., Vranjes -Duric S., Koko V., Vignjevic S., Mitrovic O. 2011: The acute effect of ethanol on adrenal cortex in female rats - possible role of nitric oxide. Alcohol Alcohol 46: 523-528
Go to original source...
Go to PubMed... - Doetze A., Satoguina J., Burchard G., Rau T., Loeliger C., Fleischer B., Hoerauf A. 2000: Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factorbeta but not by a T(h)1 to T(h)2 shift. Int. Immunol. 12: 623-630
Go to original source...
Go to PubMed... - Fournier D.B., Gordon G.B. 2000: COX-2 and colon cancer: potential targets for chemoprevention. J. Cell. Biochem. Suppl. 34: 97-102
Go to original source...
Go to PubMed... - Gately S. 2000: The contributions of cyclooxygenase-2 to tumor angiogenesis. Cancer Metastasis Rev. 19: 19-27
Go to original source...
Go to PubMed... - Gupta R.A., Dubois R.N. 2001: Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat. Rev. Cancer. 1: 11-21
Go to original source...
Go to PubMed... - Hanahan D., Weinberg R.A. 2000: The hallmarks of cancer. Cell 100: 57-70
Go to original source...
Go to PubMed... - Heiblum R., Arnon E., Gvaryahu G., Robinzon B., Snapir N. 2000: Short-term stress increases testosterone secretion from testes in male domestic fowl. Gen. Comp. Endocrinol. 120: 55-66
Go to original source...
Go to PubMed... - Herbert D.R., Orekov T., Perkins C., Finkelman F.D. 2008: IL-10 and TGF-beta redundantly protect against severe liver injury and mortality during acute schistosomiasis. J. Immunol. 181: 7214-7220
Go to original source...
Go to PubMed... - IARC Working G roup 1994: Infection with liver flukes (Opisthorchis viverrini, Opisthorchis felineus, and Clonorchis sinensis). IARC Monogr. Eval. Carcinog. Risks. Hum. 61: 121-175
Go to PubMed... - Keiser J., Utzinger J. 2005: Emerging foodborne trematodiasis. Emerg. Infect. Dis. 11: 1507-1514
Go to original source...
Go to PubMed... - Kim Y.I. 1984: Liver carcinoma and liver fluke infection. Arzneimittelforschung 34: 1121-1126
- Kim T.S., Cho S.H., Huh S., Kong Y., Sohn W.M., Hwang S.S., Chai J.Y., Lee S.H., Park Y.K., Oh D.K., Lee J.K. 2009: A nationwide survey on the prevalence of intestinal parasitic infections in the Republic of Korea, 2004. Korean J. Parasitol. 47: 37-47
Go to original source...
Go to PubMed... - Knol B.W. 1991: Stress and the endocrine hypothalamus-pituitary-testis system: a review. Vet. Q. 13: 104-114
Go to original source...
Go to PubMed... - Koga H., Sakisaka S., Ohishi M., Kawaguchi T., Taniguchi E., Sasatomi K., Harada M., Kusaba T., Tanaka M., Kimu ra R., Nakashima Y., Nakashima O., Kojiro M., Kurohiji T., Sata M. 1999: Expression of cyclooxygenase-2 in human hepatocellular carcinoma: relevance to tumor dedifferentiation. Hepatology 29: 688-696
Go to original source...
Go to PubMed... - Kondo M., Yamamoto H., Nagano H., Okami J., Ito Y., Shimizu J., Eguchi H., Miyamoto A., Dono K., Umeshita K., Matsu ura N., Wakasa K., Nakamori S., Sakon M., Monden M. 1999: Increased expression of COX-2 in nontumor liver tissue is associated with shorter disease-free survival in patients with hepatocellular arcinoma. Clin. Cancer Res. 5: 4005-4012
- Konrad L., Scheiber J.A., Schwarz L., Schrader A.J., Hofmann R. 2009: TGF-beta1 and TGF-beta2 strongly enhance the secretion of plasminogen activator inhibitor-1 and matrix metalloproteinase-9 of the human prostate cancer cell line PC3. Regul. Pept. 155: 28-32
Go to original source...
Go to PubMed... - Lee J.H., Noh J., Noh G., Choi W.S., Cho S., Lee S.S. 2011: Allergen-specific transforming growth factor-β-producing CD19(+)CD5(+) regulatory B-cell (Br3) responses in hHuman late eczematous allergic reactions to cow's milk. J. Interferon Cytokine Res. 31: 441-449
Go to original source...
Go to PubMed... - Lee J.H., Yang H.M., Bak U.B., Rim H.J. 1994: Promoting role of Clonorchis sinensis infection on induction of cholangiocarcinoma during two-step carcinogenesis. Kor. J. Parasitol. 32: 13-18
Go to original source...
Go to PubMed... - Leng J., Han C., Demetris A.J., Michalopoulos G.K., Wu T. 2003: Cyclooxygenase-2 promotes hepatocellular carcinoma cell growth through Akt activation: evidence for Akt inhibition in celecox-ibinduced apoptosis. Hepatology 38: 756-768
Go to original source...
Go to PubMed... - Lim M.K., Ju Y.H., Franceschi S., Oh J.K., Kong H.J., Hwang S.S., Park S.K., Cho S.I., Sohn W.M., Kim D.I., Yoo K.Y., Hong S.T., Shin H.R. 2006: Clonorchis sinensis infection and increasing risk of cholangiocarcinoma in the Republic of Korea. Am. J. Trop. Med. Hyg. 75: 93-96
Go to original source...
Go to PubMed... - Lun Z.R., Gasser R.B., Lai D.H., Li A.X., Zhu X.Q., Yu X.B., Fang Y.Y. 2005: Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect. Dis. 5: 31-41
Go to original source...
Go to PubMed... - Lvova M.N., Tangkawattana S., Balthaisog S., Katokhin A.V., Mordvinov V.A., Sripa B. 2012: Comparative histopathology of Opisthorchis felineus and Opisthorchis viverrini in a hamster model: an implication of high pathogenicity of the European liver fluke. Parasitol. Int. 61: 167-172
Go to original source...
Go to PubMed... - Matsui M., Rouleau V., Bruyere -Ostells L., Goarant C. 2011: Gene expression profiles of immune mediators and histopathological findings in animal models of leptospirosis: comparison between susceptible hamsters and resistant mice. Infect. Immun. 79: 4480-4492
Go to original source...
Go to PubMed... - Melby P.C., Chandrasekar B., Zhao W., Coe J.E. 2001: The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like cytokine response. J. Immunol. 166: 1912-1920
Go to original source...
Go to PubMed... - Moll H.P., Maier T., Zommer A., Lavoie T., Brostjan C. 2011: The differential activity of interferon-α subtypes is consistent among distinct target genes and cell types. Cytokine 53: 52-59.
Go to original source...
Go to PubMed... - Moller H., Heseltine E., Vainio H. 1995: Working group report on schistosomes, liver flukes and Helicobacter pylori. Int. J. Cancer. 60: 587-589
Go to original source...
Go to PubMed... - Mooradian A.D., Morley J.E., Korenman S.G. 1987: Biological actions of androgens. Endocr. Rev. 8: 1-28
Go to original source...
Go to PubMed... - Nieuwenhuizen N., Herbert D.R., Brombacher F., Lopata A.L. 2009: Differential requirements for interleukin (IL)-4 and IL-13 in protein contact dermatitis induced by Anisakis. Allergy 64: 1309-1318
Go to original source...
Go to PubMed... - Ohshima H., Tatemichi M., Sawa T. 2003: Chemical basis of inflammation-induced carcinogenesis. Arch. Biochem. Biophys. 417: 3-11
Go to original source...
Go to PubMed... - Pak J.H., Kim D.W., Moon J.H., Nam J.H., Kim J.H., Ju J.W., Kim T.S., Seo S.B. 2009: Differential gene expression profiling in human cholangiocarcinoma cells treated with Clonorchis sinensis excretory-secretory products. Parasitol. Res. 104: 1035-1046
Go to original source...
Go to PubMed... - Pentikaeinen V., Erkkilae K., Suomalainen L., Parvinen M., Dunkel L. 2000: Estradiol acts as a germ cell survival factor in the human testis in vitro. J. Clin. Endocrinol. Metab. 85: 2057-2067
Go to original source...
Go to PubMed... - Peruhype -Magalhaes V., Martins -Filho O.A., Prata A., Silva L de A., Rabello A., Teixeira-Carvalho A., Figue iredo R.M., Guimaraes -Carvalho S.F., Ferrari T.C., Van Weyenbergh J., Correa-Oliveira R. 2006: Mixed inflammatory/regulatory cytokine profile marked by simultaneous raise of interferon-gamma and interleukin-10 and low frequency of tumour necrosis factor-alpha(+) monocytes are hallmarks of active human visceral Leishmaniasis due to Leishmania chagasi infection. Clin. Exp. Immunol. 146: 124-132
Go to original source...
Go to PubMed... - Pinlaor S. 2003: 8-nitroguanine formation in the liver of hamsters infected with Opisthorchis viverrini. Biochem. Biophys. Res. Commun. 309: 567-571
Go to original source...
Go to PubMed... - Pinlaor S., Hiraku Y., Ma N., Yongvanit P., Semba R., Oikawa S., Murata M., Sripa B., Sithithaworn P., Kawanishi S. 2004a: Mechanism of NO-mediated oxidative and nitrative DNA damage in hamsters infected with Opisthorchis viverrini: a model of inflammation-mediated carcinogenesis. Nitric Oxide 11: 175-183
Go to original source...
Go to PubMed... - Pinlaor S., Ma N., Hiraku Y., Yongvanit P., Semba R., Oikawa S., Murata M., Sripa B., Sithithaworn P., Kawanishi S. 2004b: Repeated infection with Opisthorchis viverrini induces accumulation of 8-nitroguanine and 8-oxo-7, 8-dihydro-20deoxyguanine in the bile duct of hamsters via inducible nitric oxide synthase. Carcinogenesis 25: 1535-1542
Go to original source...
Go to PubMed... - Prakobwong S., Pinlaor S., Yongvanit P., Sithithaworn P., Pairojkul C., Hiraku Y. 2009: 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. 39: 825-835
Go to original source...
Go to PubMed... - Qin Z.F., Hou D.Y., Fang Y.Q., Xiao H.J., Wang J., Li K.C. 2012: Interferon-alpha enhances excitatory transmission in substantia gelatinosa neurons of rat spinal cord. Neuroimmunomodulation 19: 235-240
- Quan F.S., Cho S.W., Joo K.H. 2002: Proliferation and cytokine production of lymphocytes from Clonorchis sinensis-infected rats in response to stimulators in vitro. Chin. J. Parasitol. Parasit. Dis. 20: 136-140
- Rahman M.A., Dhar D.K., Yamaguchi E., Maruyama S., Sato T., Hayashi H., Ono T., Yamanoi A., Kohno H., Nagasue N. 2001: Coexpression of inducible nitric oxide synthase and COX-2 in hepatocellular carcinoma and surrounding liver: possible involvement of COX-2 in the angiogenesis of hepatitis C virus-positive cases. Clin. Cancer Res. 7: 1325-1332
- Rim H.J. 2005: Clonorchiasis: an update. J. Helminthol. 79: 269- 281
Go to original source...
Go to PubMed... - Samy A.S., Igwe O.J. 2012: Regulation of IL-1β-induced cyclooxygenase-2 expression by interactions of Aβ peptide, apolipoprotein E and nitric oxide in human neuroglioma. J. Mol. Neurosci. 47: 533-545
Go to original source...
Go to PubMed... - Santoro M.G. 2000: Heat shock factors and the control of the stress response. Biochem. Pharmacol. 59: 55-63
Go to original source...
Go to PubMed... - Seki S., Nakashima H., Nakashima M., Kinoshita M. 2011: Antitumor immunity produced by the liver Kupffer cells, NK cells, NKT cells, and CD8 CD122 T cells. Clin. Dev. Immunol. 2011: 868345
Go to original source...
Go to PubMed... - Sher L., Iwatsuki S., Lebeau G., Zajko A.B. 1989: Hilar cholangiocarcinoma associated with clonorchiasis. Dig. Dis. Sci. 34: 1121-1123
Go to original source...
Go to PubMed... - Shin H.R., Oh J.K., Masuyer E, Curado M.P., Bouvard V., Fang Y.Y., Wiangnon S., Sripa B., Hong S.T. 2010: Epidemiology of cholangiocarcinoma: an update focusing on risk factors. Cancer Sci. 101: 579-585
Go to original source...
Go to PubMed... - Simmons D.L., Botting R.M., Hla T. 2004: Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol. Rev. 56: 387-437
Go to original source...
Go to PubMed... - Singh B., Murphy R.F., Ding X.Z., Roginsky A.B., Bell R.H. Jr, Adrian T.E. 2007: On the role of transforming growth factor-beta in the growth inhibitory effects of retinoic acid in human pancreatic cancer cells. Mol. Cancer. 6: 82
Go to original source...
Go to PubMed... - Smirnova M.G., Kiselev S.L., Gnuchev N.V., Birchall J.P., Pearson J.P. 2002: Role of the pro-inflammatory cytokines tumor necrosis factor-alpha, interleukin-1 beta, interleukin-6 and interleukin-8 in the pathogenesis of the otitis media with effusion. Eur. Cytokine Netw. 13: 161-172
Go to PubMed... - 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. 2007: Liver fluke induces cholangiocarcinoma. PLoS Med. 4: 1148-1155
Go to original source...
Go to PubMed... - Sripa B., Mairiang E., Thinkhamrop B., Laha T., Kaewkes S., Sithithaworn P., Tessana S., Loukas A., Brindley P.J., Be thony J.M. 2009: Advanced periductal fibrosis from infection with the carcinogenic human liver fluke Opisthorchis viverrini correlates with elevated levels of interleukin-6. Hepatology 50: 1273-1281
Go to original source...
Go to PubMed... - Srivatanakul P., Sriplung H., Deerasamee S. 2004: Epidemiology of liver cancer: an overview. Asian Pac. J. Cancer Prev. 5: 118-125
Go to PubMed... - Tang T.C., Poon R.T., Lau C.P., Xie D., Fan S.T. 2005: Tumor cyclooxygenase-2 levels correlate with tumor invasiveness in human hepatocellular carcinoma. World J. Gastroenterol. 11: 1896-1902
Go to original source...
Go to PubMed... - Thornton A.M., Donovan E.E., Piccirillo C.A., Shevach E.M. 2004: Cutting edge: IL-2 is critically required for the in vitro activation of CD4+CD25+ T cell suppressor function. J. Immunol. 172: 6519-6523
Go to original source...
Go to PubMed... - Watanapa P, Watanapa W.B. 2002: Liver fluke-associated cholangiocarcinoma. Brit. J. Surg. 89: 962-970
Go to original source...
Go to PubMed... - Williams C.S., Mann M., DuBois R.N. 1999: The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18: 7908-7916
Go to original source...
Go to PubMed... - Wynn T.A. 2008: Cellular and molecular mechanisms of fibrosis. J. Pathol. 214: 199-210
Go to original source...
Go to PubMed...