DOI QR코드

DOI QR Code

ALCAM is a Novel Cytoplasmic Membrane Protein in TNF-α Stimulated Invasive Cholangiocarcinoma Cells

  • Adisakwattana, Poom (Department of Helminthology, Faculty of Tropical Medicine, Mahidol University) ;
  • Suwandittakul, Nantana (Department of Helminthology, Faculty of Tropical Medicine, Mahidol University) ;
  • Petmitr, Songsak (Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University) ;
  • Wongkham, Sopit (Department of Biochemistry, Faculty of Medicine, Khon Kaen University) ;
  • Sangvanich, Polkit (Department of Chemistry, Faculty of Science, Chulalongkorn University) ;
  • Reamtong, Onrapak (Department of Molecular Tropical Medicine and Genetics, Faculty of Tropical Medicine, Mahidol University)
  • Published : 2015.05.18

Abstract

Background: Cholangiocarcinoma (CCA), or bile duct cancer, is incurable with a high mortality rate due to a lack of effective early diagnosis and treatment. Identifying cytoplasmic membrane proteins of invasive CCA that facilitate cancer progression would contribute toward the development of novel tumor markers and effective chemotherapy. Materials and Methods: An invasive CCA cell line (KKU-100) was stimulated using TNF-${\alpha}$ and then biotinylated and purified for mass spectrometry analysis. Novel proteins expressed were selected and their mRNAs expression levels were determined by real-time RT-PCR. In addition, the expression of ALCAM was selected for further observation by Western blot analysis, immunofluorescent imaging, and antibody neutralization assay. Results: After comparing the proteomics profile of TNF-${\alpha}$ induced invasive with non-treated control cells, over-expression of seven novel proteins was observed in the cytoplasmic membrane of TNF-${\alpha}$ stimulated CCA cells. Among these, ALCAM is a novel candidate which showed significant higher mRNA- and protein levels. Immunofluorescent assay also supported that ALCAM was expressed on the cell membrane of the cancer, with increasing intensity associated with TNF-${\alpha}$. Conclusions: This study indicated that ALCAM may be a novel protein candidate expressed on cytoplasmic membranes of invasive CCA cells that could be used as a biomarker for development of diagnosis, prognosis, and drug or antibody-based targeted therapies in the future.

Keywords

References

  1. Abraham SC, Lee JH, Hruban RH, et al (2003). Molecular and immunohistochemical analysis of intraductal papillary neoplasms of the biliary tract. Hum Pathol, 34, 902-10. https://doi.org/10.1016/S0046-8177(03)00337-X
  2. Anderson CD, Pinson CW, Berlin J, et al (2004). Diagnosis and treatment of cholangiocarcinoma. Oncologist, 9, 43-57.
  3. Balkwill F (2009). Tumour necrosis factor and cancer. Nat Rev Cancer, 9, 361-71. https://doi.org/10.1038/nrc2628
  4. Bao C, Namgung H, Lee J, et al (2014). Daidzein suppresses tumor necrosis factor-alpha induced migration and invasion by inhibiting hedgehog/Gli1 signaling in human breast cancer cells. J Agric Food Chem, 62, 3759-67. https://doi.org/10.1021/jf500231t
  5. Bendas G, Borsig L (2012). Cancer cell adhesion and metastasis: selectins, integrins, and the inhibitory potential of heparins. Int J Cell Biol, 2012, 676731.
  6. Burkhardt M, Mayordomo E, Winzer KJ, et al (2006). Cytoplasmic overexpression of ALCAM is prognostic of disease progression in breast cancer. J Clin Pathol, 59, 403-9. https://doi.org/10.1136/jcp.2005.028209
  7. Campling BG, Pym J, Baker HM, et al (1991). Chemosensitivity testing of small cell lung cancer using the MTT assay. Br J Cancer, 63, 75-83. https://doi.org/10.1038/bjc.1991.16
  8. Chainuvati T, Paosawadhi A, Sripranoth M, et al (1976). Carcinoma of the cystic duct associated with opisthorchiasis. Southeast Asian J Trop Med Public Health, 7, 482-6.
  9. Cliffe LJ, Potten CS, Booth CE, et al (2007). An increase in epithelial cell apoptosis is associated with chronic intestinal nematode infection. Infect Immun, 75, 1556-64. https://doi.org/10.1128/IAI.01375-06
  10. Davies S, Jiang WG (2010). ALCAM, activated leukocyte cell adhesion molecule, influences the aggressive nature of breast cancer cells, a potential connection to bone metastasis. Anticancer Res, 30, 1163-8.
  11. Faca VM, Hanash SM (2009). In-depth proteomics to define the cell surface and secretome of ovarian cancer cells and processes of protein shedding. Cancer Res, 69, 728-30. https://doi.org/10.1158/0008-5472.CAN-08-3087
  12. Falkensammer C, Johrer K, Gander H, et al (2006). IL-4 inhibits the TNF-alpha induced proliferation of renal cell carcinoma (RCC) and cooperates with TNF-alpha to induce apoptotic and cytokine responses by RCC: implications for antitumor immune responses. Cancer Immunol Immunother, 55, 1228-37. https://doi.org/10.1007/s00262-006-0122-1
  13. Franceschini A, Szklarczyk D, Frankild S, et al (2013). STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res, 41, 808-15. https://doi.org/10.1093/nar/gks1094
  14. Fujiwara K, Ohuchida K, Sada M, et al (2014). CD166/ALCAM expression is characteristic of tumorigenicity and invasive and migratory activities of pancreatic cancer cells. PLoS One, 9, 107247. https://doi.org/10.1371/journal.pone.0107247
  15. Furubo S, Harada K, Shimonishi T, et al (1999). Protein expression and genetic alterations of p53 and ras in intrahepatic cholangiocarcinoma. Histopathology, 35, 230-40. https://doi.org/10.1046/j.1365-2559.1999.00705.x
  16. Hallermalm K, Seki K, Wei C, et al (2001). Tumor necrosis factor-alpha induces coordinated changes in major histocompatibility class I presentation pathway, resulting in increased stability of class I complexes at the cell surface. Blood, 98, 1108-15. https://doi.org/10.1182/blood.V98.4.1108
  17. Han ZD, Bi XC, Qin WJ, et al (2009). CD147 expression indicates unfavourable prognosis in prostate cancer. Pathol Oncol Res, 15, 369-74. https://doi.org/10.1007/s12253-008-9131-z
  18. Hansen AG, Arnold SA, Jiang M, et al (2014). ALCAM/CD166 is a TGF-beta-responsive marker and functional regulator of prostate cancer metastasis to bone. Cancer Res, 74, 1404-15.
  19. Hansen AG, Freeman TJ, Arnold SA, et al (2013). Elevated ALCAM shedding in colorectal cancer correlates with poor patient outcome. Cancer Res, 73, 2955-64. https://doi.org/10.1158/0008-5472.CAN-12-2052
  20. Haswell-Elkins MR, Sithithaworn P, Elkins D (1992). Opisthorchis viverrini and cholangiocarcinoma in Northeast Thailand. Parasitol Today, 8, 86-9. https://doi.org/10.1016/0169-4758(92)90241-S
  21. Huhtinen K, Suvitie P, Hiissa J, et al (2009). Serum HE4 concentration differentiates malignant ovarian tumours from ovarian endometriotic cysts. Br J Cancer, 100, 1315-9. https://doi.org/10.1038/sj.bjc.6605011
  22. Ishihama Y, Oda Y, Tabata T, et al (2005). Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics, 4, 1265-72. https://doi.org/10.1074/mcp.M500061-MCP200
  23. Jannie KM, Stipp CS, Weiner JA (2012). ALCAM regulates motility, invasiveness, and adherens junction formation in uveal melanoma cells. PLoS One, 7, 39330. https://doi.org/10.1371/journal.pone.0039330
  24. Jiao J, Hindoyan A, Wang S, et al (2012). Identification of CD166 as a surface marker for enriching prostate stem/progenitor and cancer initiating cells. PLoS One, 7, 42564. https://doi.org/10.1371/journal.pone.0042564
  25. Kischel P, Guillonneau F, Dumont B, et al (2008). Cell membrane proteomic analysis identifies proteins differentially expressed in osteotropic human breast cancer cells. Neoplasia, 10, 1014-20. https://doi.org/10.1593/neo.08570
  26. Kondo J, Sato F, Kusumi T, et al (2008). Claudin-1 expression is induced by tumor necrosis factor-alpha in human pancreatic cancer cells. Int J Mol Med, 22, 645-9.
  27. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods, 25, 402-8. https://doi.org/10.1006/meth.2001.1262
  28. Liu X, Zhang M, Go VL, et al (2010). Membrane proteomic analysis of pancreatic cancer cells. J Biomed Sci, 17, 74. https://doi.org/10.1186/1423-0127-17-74
  29. Mon NN, Kokuryo T, Hamaguchi M (2009). Inflammation and tumor progression: a lesson from TNF-alpha-dependent FAK signaling in cholangiocarcinoma. Methods Mol Biol, 512, 279-93. https://doi.org/10.1007/978-1-60327-530-9_15
  30. Moore RJ, Owens DM, Stamp G, et al (1999). Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med, 5, 828-31. https://doi.org/10.1038/10552
  31. Pinlaor S, Prakobwong S, Hiraku Y, et al (2010). Reduction of periductal fibrosis in liver fluke-infected hamsters after long-term curcumin treatment. Eur J Pharmacol, 638, 134-41. https://doi.org/10.1016/j.ejphar.2010.04.018
  32. Robbs BK, Lucena PI, Viola JP (2013). The transcription factor NFAT1 induces apoptosis through cooperation with Ras/Raf/MEK/ERK pathway and upregulation of TNF-alpha expression. Biochim Biophys Acta, 1833, 2016-28. https://doi.org/10.1016/j.bbamcr.2013.04.003
  33. Ryu J, Ku BM, Lee YK, et al (2011). Resveratrol reduces TNF-alpha-induced U373MG human glioma cell invasion through regulating NF-kappaB activation and uPA/uPAR expression. Anticancer Res, 31, 4223-30.
  34. Song W, Tian L, Li SS, et al (2014). The aberrant expression and localization of prohibitin during apoptosis of human cholangiocarcinoma Mz-ChA-1 cells. FEBS Lett, 588, 422-8. https://doi.org/10.1016/j.febslet.2013.12.021
  35. Srimunta U, Sawanyawisuth K, Kraiklang R, et al (2012). High expression of ABCC1 indicates poor prognosis in intrahepatic cholangiocarcinoma. Asian Pac J Cancer Prev, 13, 125-30.
  36. Sripa B, Pairojkul C (2008). Cholangiocarcinoma: lessons from Thailand. Curr Opin Gastroenterol, 24, 349-56. https://doi.org/10.1097/MOG.0b013e3282fbf9b3
  37. Srivatanakul P, Sriplung H, Deerasamee S (2004). Epidemiology of liver cancer: an overview. Asian Pac J Cancer Prev, 5, 118-25.
  38. Tachezy M, Zander H, Marx AH, et al (2012). ALCAM (CD166) expression and serum levels in pancreatic cancer. PLoS One, 7, 39018. https://doi.org/10.1371/journal.pone.0039018
  39. Tanimura Y, Kokuryo T, Tsunoda N, et al (2005). Tumor necrosis factor alpha promotes invasiveness of cholangiocarcinoma cells via its receptor, TNFR2. Cancer Lett, 219, 205-13. https://doi.org/10.1016/j.canlet.2004.07.027
  40. Techasen A, Namwat N, Loilome W, et al (2014). Tumor necrosis factor-alpha modulates epithelial mesenchymal transition mediators ZEB2 and S100A4 to promote cholangiocarcinoma progression. J Hepatobiliary Pancreat Sci, 21, 703-11. https://doi.org/10.1002/jhbp.125
  41. Wang SL, Li YX, Song YW, et al (2011). Triple-negative or HER2-positive status predicts higher rates of locoregional recurrence in node-positive breast cancer patients after mastectomy. Int J Radiat Oncol Biol Phys, 80, 1095-101. https://doi.org/10.1016/j.ijrobp.2010.03.038
  42. Wiiger MT, Gehrken HB, Fodstad O, et al (2010). A novel human recombinant single-chain antibody targeting CD166/ALCAM inhibits cancer cell invasion in vitro and in vivo tumour growth. Cancer Immunol Immunother, 59, 1665-74. https://doi.org/10.1007/s00262-010-0892-3
  43. Wright GL, Jr., Haley C, Beckett ML, et al (1995). Expression of prostate-specific membrane antigen in normal, benign, and malignant prostate tissues. Urol Oncol, 1, 18-28. https://doi.org/10.1016/1078-1439(95)00002-Y
  44. Yonglitthipagon P, Pairojkul C, Chamgramol Y, et al (2010). Up-regulation of annexin A2 in cholangiocarcinoma caused by Opisthorchis viverrini and its implication as a prognostic marker. Int J Parasitol, 40, 1203-12. https://doi.org/10.1016/j.ijpara.2010.05.002
  45. Zhou JX, Li Y, Chen SX, et al (2011). Expression and prognostic significance of cancer-testis antigens (CTA) in intrahepatic cholagiocarcinoma. J Exp Clin Cancer Res, 30, 2. https://doi.org/10.1186/1756-9966-30-2
  46. Ziegler YS, Moresco JJ, Tu PG, et al (2014). Plasma membrane proteomics of human breast cancer cell lines identifies potential targets for breast cancer diagnosis and treatment. PLoS One, 9, 102341. https://doi.org/10.1371/journal.pone.0102341

Cited by

  1. Molecular characterization of serine protease inhibitor isoform 3, SmSPI, from Schistosoma mansoni vol.115, pp.8, 2016, https://doi.org/10.1007/s00436-016-5053-y
  2. Biomarkers for the Diagnosis of Cholangiocarcinoma: A Systematic Review vol.98, pp.6, 2018, https://doi.org/10.4269/ajtmh.17-0879