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Article

Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells

  • Authors:
    • Ga Rim Kim
    • Ga-Hee Ha
    • Jae-Ho Bae
    • Sae-Ock Oh
    • Sun-Hee Kim
    • Chi-Dug Kang
  • View Affiliations / Copyright

    Affiliations: Department of Biochemistry, Pusan National University School of Medicine, Yangsan, Gyeongsangnam‑do 626-870, Republic of Korea, Department of Anatomy, Pusan National University School of Medicine, Yangsan, Gyeongsangnam‑do 626-870, Republic of Korea
  • Pages: 1641-1646
    |
    Published online on: January 29, 2015
       https://doi.org/10.3892/ol.2015.2918
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Abstract

In the present study, the soft agar clonogenicity and the susceptibility of clonogenic cancer cells to natural killer (NK) cells were compared between primary colon cancer cells (KM12C) and metastatic colon cancer cells (KM12L4a and KM12SM) to determine whether the metastatic cancer cells consisted of more cancer stem‑like cells and were resistant to NK cell‑mediated lysis. The majority of colon cancer cells were positive for putative cancer stem cell markers, including CD44, CD133 and EpCAM, with the exception of KM12C cells, of which only ~55% were positive for CD133. In addition, the expression levels of sex determining region Y‑box 2, Nanog and octamer‑binding transcription factor 4, which are essential for maintaining self‑renewal, were higher in KM12L4a and KM12SM compared with that in KM12C cells. Consistently, an increased clonogenicity of KM12L4a and KM12SM compared with KM12C cells in soft agar was observed. The expression levels of NKG2D ligands, including major histocompatibility complex class I polypeptide‑related sequence A/B and UL16 binding protein 2, and of death receptor 5 were significantly higher in KM12L4a and KM12SM than in KM12C cells. Furthermore, the results indicated an increased susceptibility of KM12L4a and KM12SM to NK cell‑mediated cytotoxicity in comparison with KM12C cells. These results indicated that metastatic colon cancer cell populations may consist of more cancer stem‑like cells, and have greater susceptibility to NK cell‑mediated lysis compared with that of primary colon cancers.
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1 

Gupta GP and Massagué J: Cancer metastasis: building a framework. Cell. 127:679–695. 2006. View Article : Google Scholar : PubMed/NCBI

2 

Chaffer CL and Weinberg RA: A perspective on cancer cell metastasis. Science. 331:1559–1564. 2011. View Article : Google Scholar : PubMed/NCBI

3 

Fanali C, Lucchetti D, Farina M, et al: Cancer stem cells in colorectal cancer from pathogenesis to therapy: controversies and perspectives. World J Gastroenterol. 20:923–42. 2014. View Article : Google Scholar : PubMed/NCBI

4 

Chen K, Huang YH and Chen JL: Understanding and targeting cancer stem cells: therapeutic implications and challenges. Acta Pharmacol Sin. 34:732–740. 2013. View Article : Google Scholar : PubMed/NCBI

5 

Clevers H: The cancer stem cell: premises, promises and challenges. Nat Med. 17:313–319. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Xie K, Huang S, Dong Z, Gutman M and Fidler IJ: Direct correlation between expression of endogenous inducible nitric oxide synthase and regression of M5076 reticulum cell sarcoma hepatic metastases in mice treated with liposomes containing lipopeptide CGP 31362. Cancer Res. 55:3123–3131. 1995.PubMed/NCBI

7 

Wong CW, Lee A, Shientag L, et al: Apoptosis: an early event in metastatic inefficiency. Cancer Res. 61:333–338. 2001.PubMed/NCBI

8 

Oliver L, Cordel S, Barbieux I, et al: Resistance to apoptosis is increased during metastatic dissemination of colon cancer. Clin Exp Metastasis. 19:175–180. 2002. View Article : Google Scholar : PubMed/NCBI

9 

Ljunggren HG and Malmberg KJ: Prospects for the use of NK cells in immunotherapy of human cancer. Nat Rev Immunol. 7:329–339. 2007. View Article : Google Scholar : PubMed/NCBI

10 

Malmberg KJ, Bryceson YT, Carlsten M, et al: NK cell-mediated targeting of human cancer and possibilities for new means of immunotherapy. Cancer Immunol Immunother. 57:1541–1552. 2008. View Article : Google Scholar : PubMed/NCBI

11 

Smyth MJ, Cretney E, Kelly JM, et al: Activation of NK cell cytotoxicity. Mol Immunol. 42:501–510. 2005. View Article : Google Scholar

12 

Micheau O, Shirley S and Dufour F: Death receptors as targets in cancer. Br J Pharmacol. 169:1723–1744. 2013. View Article : Google Scholar : PubMed/NCBI

13 

Long EO, Kim HS, Liu D, Peterson ME and Rajagopalan S: Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol. 31:227–258. 2013. View Article : Google Scholar : PubMed/NCBI

14 

Chan CJ, Smyth MJ and Martinet L: Molecular mechanisms of natural killer cell activation in response to cellular stress. Cell Death Differ. 21:5–14. 2014. View Article : Google Scholar

15 

Morikawa K, Walker SM, Nakajima M, Pathak S, Jessup JM and Fidler IJ: Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res. 48:6863–6871. 1988.PubMed/NCBI

16 

Elkins K, Zheng B, Go M, et al: FcRL5 as a target of antibody-drug conjugates for the treatment of multiple myeloma. Mol Cancer Ther. 11:2222–2232. 2012. View Article : Google Scholar : PubMed/NCBI

17 

Hennel R, Brix N, Seidl K, et al: Release of monocyte migration signals by breast cancer cell lines after ablative and fractionated γ-irradiation. Radiat Oncol. 9:852014. View Article : Google Scholar

18 

Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar

19 

Jaenisch R and Young R: Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell. 132:567–582. 2008. View Article : Google Scholar : PubMed/NCBI

20 

Hamburger AW and Salmon SE: Primary bioassay of human tumor stem cells. Science. 197:461–463. 1977. View Article : Google Scholar : PubMed/NCBI

21 

Um JH, Kwon JK, Kang CD, et al: Relationship between antiapoptotic molecules and metastatic potency and the involvement of DNA-dependent protein kinase in the chemosensitization of metastatic human cancer cells by epidermal growth factor receptor blockade. J Pharmacol Exp Ther. 311:1062–1070. 2004. View Article : Google Scholar : PubMed/NCBI

22 

Alison MR, Lim SM and Nicholson LJ: Cancer stem cells: problems for therapy? J Pathol. 223:147–161. 2011. View Article : Google Scholar

23 

Camps J, Morales C, Prat E, et al: Genetic evolution in colon cancer KM12 cells and metastatic derivates. Int J Cancer. 110:869–874. 2004. View Article : Google Scholar : PubMed/NCBI

24 

De Lange R, Burtscher H, Jarsch M and Weidle UH: Identification of metastasis-associated genes by transcriptional profiling of metastatic versus non-metastatic colon cancer cell lines. Anticancer Res. 21:2329–2339. 2001.PubMed/NCBI

25 

Saigusa S, Tanaka K, Toiyama Y, et al: Correlation of CD133, OCT4, and SOX2 in rectal cancer and their association with distant recurrence after chemoradiotherapy. Ann Surg Oncol. 16:3488–3498. 2009. View Article : Google Scholar : PubMed/NCBI

26 

O’Brien CA, Pollett A, Gallinger S and Dick JE: A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 445:106–110. 2007. View Article : Google Scholar

27 

Ricci-Vitiani L, Lombardi DG, Pilozzi E, et al: Identification and expansion of human colon-cancer-initiating cells. Nature. 445:111–115. 2007. View Article : Google Scholar

28 

Elsaba TM, Martinez-Pomares L, Robins AR, et al: The stem cell marker CD133 associates with enhanced colony formation and cell motility in colorectal cancer. PLoS One. 5:e107142010. View Article : Google Scholar : PubMed/NCBI

29 

Shmelkov SV, Butler JM, Hooper AT, et al: CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest. 118:2111–2120. 2008.PubMed/NCBI

30 

LaBarge MA and Bissell MJ: Is CD133 a marker of metastatic colon cancer stem cells? J Clin Invest. 118:2021–2024. 2008.PubMed/NCBI

31 

Dalerba P, Dylla SJ, Park IK, et al: Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA. 104:10158–10163. 2007. View Article : Google Scholar : PubMed/NCBI

32 

Terunuma H, Deng X, Dewan Z, Fujimoto S and Yamamoto N: Potential role of NK cells in the induction of immune responses: implications for NK cell-based immunotherapy for cancers and viral infections. Int Rev Immunol. 27:93–110. 2008. View Article : Google Scholar : PubMed/NCBI

33 

Fernández-Messina L, Reyburn HT and Valés-Gómez M: Human NKG2D-ligands: cell biology strategies to ensure immune recognition. Front Immunol. 3:2992012. View Article : Google Scholar : PubMed/NCBI

34 

Kim JY, Son YO, Park SW, et al: Increase of NKG2D ligands and sensitivity to NK cell-mediated cytotoxicity of tumor cells by heat shock and ionizing radiation. Exp Mol Med. 38:474–484. 2006. View Article : Google Scholar : PubMed/NCBI

35 

Kim JY, Bae JH, Lee SH, et al: Induction of NKG2D ligands and subsequent enhancement of NK cell-mediated lysis of cancer cells by arsenic trioxide. J Immunother. 31:475–486. 2008. View Article : Google Scholar : PubMed/NCBI

36 

Bae JH, Kim SJ, Kim MJ, et al: Susceptibility to natural killer cell-mediated lysis of colon cancer cells is enhanced by treatment with epidermal growth factor receptor inhibitors through UL16-binding protein-1 induction. Cancer Sci. 103:7–16. 2012. View Article : Google Scholar

37 

Raulet DH, Gasser S, Gowen BG, et al: Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol. 31:413–441. 2013. View Article : Google Scholar : PubMed/NCBI

38 

McGilvray RW, Eagle RA, Watson NF, et al: NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin Cancer Res. 15:6993–7002. 2009. View Article : Google Scholar : PubMed/NCBI

39 

Sheard MA, Asgharzadeh S, Liu Y, et al: Membrane-bound TRAIL supplements natural killer cell cytotoxicity against neuroblastoma cells. J Immunother. 36:319–329. 2013. View Article : Google Scholar : PubMed/NCBI

40 

Tallerico R, Todaro M, Di Franco S, et al: Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. J Immunol. 190:2381–2390. 2013. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Kim GR, Ha G, Bae J, Oh S, Kim S and Kang C: Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells. Oncol Lett 9: 1641-1646, 2015.
APA
Kim, G.R., Ha, G., Bae, J., Oh, S., Kim, S., & Kang, C. (2015). Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells. Oncology Letters, 9, 1641-1646. https://doi.org/10.3892/ol.2015.2918
MLA
Kim, G. R., Ha, G., Bae, J., Oh, S., Kim, S., Kang, C."Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells". Oncology Letters 9.4 (2015): 1641-1646.
Chicago
Kim, G. R., Ha, G., Bae, J., Oh, S., Kim, S., Kang, C."Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells". Oncology Letters 9, no. 4 (2015): 1641-1646. https://doi.org/10.3892/ol.2015.2918
Copy and paste a formatted citation
x
Spandidos Publications style
Kim GR, Ha G, Bae J, Oh S, Kim S and Kang C: Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells. Oncol Lett 9: 1641-1646, 2015.
APA
Kim, G.R., Ha, G., Bae, J., Oh, S., Kim, S., & Kang, C. (2015). Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells. Oncology Letters, 9, 1641-1646. https://doi.org/10.3892/ol.2015.2918
MLA
Kim, G. R., Ha, G., Bae, J., Oh, S., Kim, S., Kang, C."Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells". Oncology Letters 9.4 (2015): 1641-1646.
Chicago
Kim, G. R., Ha, G., Bae, J., Oh, S., Kim, S., Kang, C."Metastatic colon cancer cell populations contain more cancer stem‑like cells with a higher susceptibility to natural killer cell‑mediated lysis compared with primary colon cancer cells". Oncology Letters 9, no. 4 (2015): 1641-1646. https://doi.org/10.3892/ol.2015.2918
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