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Increased cell proliferation of mouse fibroblast NIH-3T3 in vitro induced by excretory/secretory product(s) from Opisthorchis viverrini

Published online by Cambridge University Press:  14 September 2004

C. THUWAJIT ,
P. THUWAJIT ,
S. KAEWKES ,
B. SRIPA ,
K. UCHIDA ,
M. MIWA  and
S. WONGKHAM
C. THUWAJIT
Affiliation:
Department of Biochemistry, Khon Kaen University, Khon Kaen 40002, Thailand Liver fluke and Cholangiocarcinoma Research Center, Khon Kaen University, Khon Kaen 40002, Thailand
P. THUWAJIT
Affiliation:
Department of Biochemistry, Khon Kaen University, Khon Kaen 40002, Thailand Liver fluke and Cholangiocarcinoma Research Center, Khon Kaen University, Khon Kaen 40002, Thailand
S. KAEWKES
Affiliation:
Department of Parasitology, Khon Kaen University, Khon Kaen 40002, Thailand Liver fluke and Cholangiocarcinoma Research Center, Khon Kaen University, Khon Kaen 40002, Thailand
B. SRIPA
Affiliation:
Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand Liver fluke and Cholangiocarcinoma Research Center, Khon Kaen University, Khon Kaen 40002, Thailand
K. UCHIDA
Affiliation:
Department of Biochemistry and Molecular Oncology, Institute of Basic Medical Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
M. MIWA
Affiliation:
Department of Biochemistry and Molecular Oncology, Institute of Basic Medical Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
S. WONGKHAM
Affiliation:
Department of Biochemistry, Khon Kaen University, Khon Kaen 40002, Thailand Liver fluke and Cholangiocarcinoma Research Center, Khon Kaen University, Khon Kaen 40002, Thailand
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Abstract

Infection by Opisthorchis viverrini is a strong risk factor for cholangiocarcinoma. However, the mechanism by which the parasite is involved in carcinogenesis is not clear. In addition to the direct damage of the bile duct epithelium via direct contact with O. viverrini, the excretory/secretory (ES) product(s) released from the parasites may play important roles in this process. We therefore investigated the responses of a fibroblast cell line, NIH-3T3, to ES product(s) released from O. viverrini by using a non-contact co-culture technique. In this culture system, the parasites in the upper chamber had no direct contact with the NIH-3T3 cells in the lower chamber of the culture plate. The results indicated a marked increase in NIH-3T3 cell proliferation in the non-contact co-culture condition with either 0% or 10% calf serum in the medium compared with that without parasites. ES product(s) increased cell proliferation by stimulating the expression of phosphorylated retinoblastoma (pRB) and cyclin D1, the key proteins in driving cells through the G1/S transition point of the cell cycle. This led to the induction of cells going into the S-phase of the cell cycle. ES product(s) also changed the morphology of NIH-3T3 cells to a refractive and narrow shape, which allowed the cells to proliferate in the limited culture area. For the first time, we have been able to demonstrate increased cell proliferation induced by the ES product(s) from O. viverrini; this finding may clarify how O. viverrini ES product(s) affect human bile duct epithelium during cholangiocarcinogenesis.

Keywords

Opisthorchis viverriniexcretory/secretory product(s)NIH-3T3non-contact co-culturecell proliferationcell cycle
Type
Research Article
Information
Parasitology , Volume 129 , Issue 4 , October 2004 , pp. 455 - 464
Copyright
2004 Cambridge University Press

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References

REFERENCES

BHAMARAPRAVATI, N., THAMMAVIT, W. & VAJRASTHIRA, S. (1978). Liver changes in hamsters infected with a liver fluke of man, Opisthorchis viverrini. American Journal of Tropical Medicine and Hygiene 27, 787–794.CrossRefGoogle Scholar
DANESH, F. R., YE, M., SALMI, S., LAPOINTE, M. & BATLLE, D. (1999). Temporal profile of serum-induced S-phase entry and retinoblastoma protein phosphorylation in human skin fibroblasts. Kidney International 56, 1282–1285.CrossRefGoogle Scholar
DISALVO, C. V., ZHANG, D. & JACOBBERGER, J. W. (1995). Regulation of NIH-3T3 cell G1 phase transit by serum during exponential growth. Cell Proliferation 28, 511–524.CrossRefGoogle Scholar
GILLE, H. & DOWNWARD, J. (1999). Multiple ras effector pathways contribute to G(1) cell cycle progression. Journal of Biological Chemistry 274, 22033–22040.CrossRefGoogle Scholar
GROSSI, M., LA ROCCA, S. A., PIERLUIGI, G., VANNUCCHI, S., RUARO, E. M., SCHNEIDER, C. & TATO, F. (1998). Role of Gas1 down-regulation in mitogenic stimulation of quiescent NIH3T3 cells by v-Src. Oncogene 17, 1629–1638.CrossRefGoogle Scholar
INTERNATIONAL AGENCY FOR RESEARCH ON CANCER (1994). Infection with the liver flukes (Opisthorchis viverrini, Opisthorchis felineus and Clonorchis sinensis). IARC Monograp on Evaluation of Carcinogenic Risks of Human 61, 121–175.
IYER, V. R., EISEN, M. B., ROSS, D. T., SCHULER, G., MOORE, T., LEE, J. C., TRENT, J. M., STAUDT, L. M., HUDSON, J. Jr., BOGUSKI, M. S., LASHKARI, D., SHALON, D., BOTSTEIN, D. & BROWN, P. O. (1999). The transcriptional program in the response of human fibroblasts to serum. Science 283, 83–87.CrossRefGoogle Scholar
JONGSUKSUNTIGUL, P. & IMSOMBOON, T. (1998). Epidemiology of opisthorchiasis and national control program in Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 29, 327–332.Google Scholar
KERKHOFF, E. & RAPP, U. R. (1997). Induction of cell proliferation in quiescent NIH 3T3 cells by oncogenic c-Raf-1. Molecular and Cellular Biology 17, 2576–2586.CrossRefGoogle Scholar
KIERSZENBAUM, F., CUNA, W. R., BELTZ, L. A. & SZTEIN, M. B. (1990). Trypanosomal immunosuppressive factor: a secretion product(s) of Trypanosoma cruzi that inhibits proliferation and IL-2 receptor expression by activated human peripheral blood mononuclear cells. Journal of Immunology 144, 4000–4004.Google Scholar
MATSUSHIME, H., QUELLE, D. E., SHURTLEFF, S. A., SHIBUYA, M., SHERR, C. J. & KATO, J. Y. (1994). D-type cyclin-dependent kinase activity in mammalian cells. Molecular and Cellular Biology 14, 2066–2076.CrossRefGoogle Scholar
MIGASENA, P., REAUNSUWAN, W. & CHANGBUMRUNG, S. (1980). Nitrates and nitrites in local Thai preserved protein foods. Journal of Medical Association of Thailand 63, 500–505.Google Scholar
MITACEK, E. J., BRUNNEMANN, K. D., SUTTAJIT, M., MARTIN, N., LIMSILA, T., OHSHIMA, H. & CAPLAN, L. S. (1999). Exposure to N-nitroso compounds in a population of high liver cancer regions in Thailand: volatile nitrosamine (VNA) levels in Thai food. Food and Chemical Toxicology 37, 297–305.CrossRefGoogle Scholar
NORBURY, C. & NURSE, P. (1992). Animal cell cycles and their control. Annual Review of Biochemistry 61, 441–470.CrossRefGoogle Scholar
PAIROJKUL, C., SHIRAI, T., HIROHASHI, S., THAMAVIT, W., BHUDHISAWAT, W., UTTARAVICIEN, T., ITOH, M. & ITO, N. (1991). Multistage carcinogenesis of liver-fluke-associated cholangiocarcinoma in Thailand. Princess Takamatsu Symposium 22, 77–86.Google Scholar
PARKIN, D. M., SRIVATANAKUL, P., KHLAT, M., CHENVIDHYA, D., CHOTIWAN, P., INSIRIPONG, S., L'ABBE, K. A. & WILD, C. P. (1991). Liver cancer in Thailand. I. A case-control study of cholangiocarcinoma. International Journal of Cancer 48, 323–328.Google Scholar
PATTANAPANYASAT, K., FLAVELL, D. J. & VONGSANGNAK, V. (1983). A method for collecting metacercariae of Opisthorchis viverrini. Siriraj Hospital Gazette 35, 143–146.Google Scholar
PINLAOR, S., YONGVANIT, P., HIRAKU, Y., MA, N., SEMBA, R., OIKAWA, S., MURATA, M., SRIPA, B., SITHITHAWORN, P. & KAWANISHI, S. (2003). 8-Nitroguanine formation in the liver of hamsters infected with Opisthorchis viverrini. Biochemical and Biophysical Research Communications 309, 567–571.CrossRefGoogle Scholar
PLANAS-SILVA, M. D. & WEINBERG, R. A. (1997). The restriction point and control of cell proliferation. Current Opinion in Cell Biology 9, 768–772.CrossRefGoogle Scholar
RIGANTI, M., PUNGPAK, S., PUNPOOWONG, B., BUNNAG, D. & HARINASUTA, T. (1989). Human pathology of Opisthorchis viverrini infection: a comparison of adults and children. Southeast Asian Journal of Tropical Medicine and Public Health 20, 95–100.Google Scholar
SHERR, C. J. & ROBERTS, J. M. (1995). Inhibitors of mammalian G1 cyclin-dependent kinases. Genes and Development 9, 1149–1163.CrossRefGoogle Scholar
SHERR, C. J. (1996). Cancer cell cycles. Science 274, 1672–1677.CrossRefGoogle Scholar
SPENCER, J. A. & MISRA, R. P. (1999). Expression of the SRF gene occurs through a Ras/Sp/SRF-mediated-mechanism in response to serum growth signals. Oncogene 18, 7319–7327.CrossRefGoogle Scholar
TAYLOR, S. J. & SHALLOWAY, D. (1996). Cell cycle-dependent activation of Ras. Current Biology 6, 1621–1627.CrossRefGoogle Scholar
VATANASAPT, V., SRIPA, B., SITHITHAWORN, P. & MAIRIANG, P. (1999). Liver flukes and liver cancer. Cancer Survey 33, 313–343.Google Scholar
WATANAPA, P. & WATANAPA, W. B. (2002). Liver fluke-associated cholangiocarcinoma. British Journal of Surgery 89, 962–970.CrossRefGoogle Scholar
WATANAPA, P. & WILLIAMSON, R. C. (1993). Experimental pancreatic hyperplasia and neoplasia: effects of dietary and surgical manipulation. British Journal of Cancer 67, 877–884.CrossRefGoogle Scholar
WILLIAMSON, R. C. N. & RAINEY, J. B. (1984). The relationship between intestinal hyperplasia and carcinogenesis. Scandinavian Journal of Gastroenterology 19 (Suppl.), 57–76.Google Scholar