Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Identification of a Cancer Stem-like Population in the Lewis Lung Cancer Cell Line

  • Zhang, An-Mei (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Fan, Ye (Institute of Respiratory Diseases, Xinqiao Hospital, Third Military Medical University) ;
  • Yao, Quan (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Ma, Hu (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Lin, Sheng (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Zhu, Cong-Hui (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Wang, Xin-Xin (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Liu, Jia (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Zhu, Bo (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Sun, Jian-Guo (Institute of Cancer, Xinqiao Hospital, Third Military Medical University) ;
  • Chen, Zheng-Tang (Institute of Cancer, Xinqiao Hospital, Third Military Medical University)
  • Published : 2012.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Although various human cancer stem cells (CSCs) have been defined, their applications are restricted to immunocompromised models. Developing a novel CSC model which could be used in immunocompetent or transgenic mice is essential for further understanding of the biomolecular characteristics of tumor stem cells. Therefore, in this study, we analyzed murine lung cancer cells for the presence of CSCs. Methods: Side population (SP) cells were isolated by fluorescence activated cell sorting, followed by serum-free medium (SFM) culture, using Lewis lung carcinoma cell (LLC) line. The self-renewal, differentiated progeny, chemosensitivity, and tumorigenic properties in SP and non-SP cells were investigated through in vitro culture and in vivo serial transplantation. Differential expression profiles of stem cell markers were examined by RT-PCR. Results: The SP cell fraction comprised 1.1% of the total LLC population. SP cells were available to grow in SFM, and had significantly enhanced capacity for cell proliferation and colony formation. They were also more resistant to cisplatin in comparison to non-SP cells, and displayed increased tumorigenic ability. Moreover, SP cells showed higher mRNA expression of Oct-4, ABCG2, and CD44. Conclusion: We identified SP cells from a murine lung carcinoma, which possess well-known characteristics of CSCs. Our study established a useful model that should allow investigation of the biological features and pharmacosensitivity of lung CSCs, both in vitro and in syngeneic immunocompetent or transgenic/knockout mice.

Keywords

References

  1. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al (2003). Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA, 100, 3983-8. https://doi.org/10.1073/pnas.0530291100
  2. Broadley KW, Hunn MK, Farrand KJ, et al (2011). Side population is not necessary or sufficient for a cancer stem cell phenotype in glioblastoma multiforme. Stem Cells, 29, 452-61. https://doi.org/10.1002/stem.582
  3. Casares N, Pequignot MO, Tesniere A, et al (2005). Caspasedependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med, 202, 1691-701. https://doi.org/10.1084/jem.20050915
  4. Collins AT, Berry PA, Hyde C, et al (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res, 65, 10946-51. https://doi.org/10.1158/0008-5472.CAN-05-2018
  5. Collins LG, Haines C, Perkel R, Enck RE (2007). Lung cancer: diagnosis and management. Am Fam Physician, 75, 56-63.
  6. Dalerba P, Cho RW, Clarke MF (2007). Cancer stem cells: models and concepts. Annu Rev Med, m 58, 267-84.
  7. Dou J, Gu N (2010). Emerging strategies for the identification and targeting of cancer stem cells. Tumor Biol, 31, 243-53. https://doi.org/10.1007/s13277-010-0023-y
  8. Eramo A, Lotti F, Sette G, et al (2008). Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ, 15, 504-14. https://doi.org/10.1038/sj.cdd.4402283
  9. Fang D, Nguyen TK, Leishear K, et al (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res, 65, 9328-37. https://doi.org/10.1158/0008-5472.CAN-05-1343
  10. Goodell MA, Brose K, Paradis G, et al (1996). Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med, 183, 1797-806. https://doi.org/10.1084/jem.183.4.1797
  11. Ho MM, Ng AV, Lam S, Hung JY (2007). Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res, 67, 4827-33. https://doi.org/10.1158/0008-5472.CAN-06-3557
  12. Jarm T, An DJ, Belehradek JJr, et al (1997). Study of blood perfusion with Patent Blue staining method in LPB fibrosarcoma tumors in immuno-competent and immunodeficient mice after electrotherapy by direct current. Radiol Oncol, 31, 33-8.
  13. Jemal A, Tiwaei RC, Murray T, et al (2004). Cancer Stat. 2004. CA Cancer J Clin, 54, 8-29. https://doi.org/10.3322/canjclin.54.1.8
  14. Luster AD, Leder P (1993). IP-10, a CXC chemokine, elicits a potent thymus-dependent anti-tumor response in vivo. J Exp Med, 178, 1057-65. https://doi.org/10.1084/jem.178.3.1057
  15. Lukacs KV, Porter CD, Pardo OE, et al (1999). In vivo transfer of bacterial marker genes results in differing levels of gene expression and tumor progression in immunocompetent and immunodeficient mice. Hum Gene Ther, 10, 2373-9. https://doi.org/10.1089/10430349950017022
  16. Matsui W, Huff CA, Wang Q, et al (2004). Characterization of clonogenic multiple myeloma cells. Blood, 103, 2332-6. https://doi.org/10.1182/blood-2003-09-3064
  17. Mitsutake N, Iwao A, Nagai K, et al (2007). Characterization of side population in thyroid cancer cell lines: cancer stem-like cells are enriched partly but not exclusively. Endocrinology, 148, 1797-803. https://doi.org/10.1210/en.2006-1553
  18. Meng X, Li M, Wang X, et al (2009). Both CD133+ and CD133- subpopulations of A549 and H446 cells contain cancer-initiating cells. Cancer Sci, 100, 1040-6. https://doi.org/10.1111/j.1349-7006.2009.01144.x
  19. Nian WQ, Chen FL, Ao XJ, Chen ZT (2011). CXCR4 positive cells from Lewis lung carcinoma cell line have cancer metastatic stem cell characteristics. Mol Cell Biochem, 355, 241-8. https://doi.org/10.1007/s11010-011-0860-z
  20. Obeid M, Tesniere A, Ghiringhelli F, et al (2007). Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med, 13, 54-61. https://doi.org/10.1038/nm1523
  21. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007). A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature, 445, 106-10. https://doi.org/10.1038/nature05372
  22. Petersen I, Petersen S (2001). Towards a genetic-based classification of human lung cancer. Anal Cell Pathol, 22, 111-21. https://doi.org/10.1155/2001/374304
  23. Prince ME, Sivanandan R, Kaczorowski A, et al (2007). Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA, 104, 973-8. https://doi.org/10.1073/pnas.0610117104
  24. Reynolds BA, Weiss S (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol, 175, 1-13. https://doi.org/10.1006/dbio.1996.0090
  25. Reya T, Morrison SJ, Clarke MF, Weissman (2001). Stem cells, cancer, and cancer stem cells. Nature, 414, 105-11. https://doi.org/10.1038/35102167
  26. Schreiber S, Gross S, Brandis A, et al (2002). Local photodynamic therapy (PDT) of rat C6 glioma xenografts with Pdbacteriopheophorbide leads to decreased metastases and increase of animal cure compared with surgery. Int J Cancer, 99, 279-85. https://doi.org/10.1002/ijc.10299
  27. Singh SK, Hawkins C, Clarke ID, et al (2004). Identification of human brain tumour initiating cells. Nature, 432, 396-401. https://doi.org/10.1038/nature03128
  28. Seigel GM, Campbell LM, Narayan M, Gonzalez-Fernandez F (2005). Cancer stem cell characteristics in retinoblastoma. Mol Vision, 11, 729-37.
  29. Shi GM, Xu Y, Fan J, et al (2008). Identification of side population cells in human hepatocellular carcinoma cell lines with stepwise metastatic potentials. J Cancer Res Clin Oncol, 134, 1155-63. https://doi.org/10.1007/s00432-008-0407-1
  30. Sung JM, Cho HJ, Yi H, et al (2008). Characterization of a stem cell population in lung cancer A549 cells. Biochem Biophys Res Commun, 371, 163-7. https://doi.org/10.1016/j.bbrc.2008.04.038
  31. Tropepe V, Sibilia M, Ciruna BG, et al (1996). Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol, 208, 166-88.
  32. Teng Y, Wang X, Wang Y, Ma D (2010). Wnt/beta-catenin signaling regulates cancer stem cells in lung cancer A549 cells. Biochem Biophys Res Commun, 392, 373-9. https://doi.org/10.1016/j.bbrc.2010.01.028
  33. Visvader JE, Lindeman GJ (2008). Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer, 8, 755-68. https://doi.org/10.1038/nrc2499
  34. Wang J, Guo LP, Chen LZ, et al (2007). Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Res, 67, 3716-24. https://doi.org/10.1158/0008-5472.CAN-06-4343
  35. Yang ZF, Ho DW, Ng MN, et al (2008). Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell, 13, 153-66. https://doi.org/10.1016/j.ccr.2008.01.013
  36. Zhou J, Wang CY, Liu T, et al (2008). Persistence of side population cells with high drug efflux capacity in pancreatic cancer. World J Gastroenterol, 14, 925-30. https://doi.org/10.3748/wjg.14.925

Cited by

  1. All-trans-retinoic Acid Promotes Iodine Uptake Via Up-regulating the Sodium Iodide Symporter in Medullary Thyroid Cancer Stem Cells vol.15, pp.4, 2014, https://doi.org/10.7314/APJCP.2014.15.4.1859
  2. ALDH1 in Combination with CD44 as Putative Cancer Stem Cell Markers are Correlated with Poor Prognosis in Urothelial Carcinoma of the Urinary Bladder vol.15, pp.5, 2014, https://doi.org/10.7314/APJCP.2014.15.5.2013
  3. Comparative Analysis of Oct4 in Different Histological Subtypes of Esophageal Squamous Cell Carcinomas in Different Clinical Conditions vol.15, pp.8, 2014, https://doi.org/10.7314/APJCP.2014.15.8.3519
  4. Characterization of side population cells isolated from the colon cancer cell line SW480 vol.45, pp.3, 2014, https://doi.org/10.3892/ijo.2014.2498
  5. Side Population Cell Level in Human Breast Cancer and Factors Related to Disease-free Survival vol.16, pp.3, 2015, https://doi.org/10.7314/APJCP.2015.16.3.991
  6. Photodynamic Therapy-mediated Cancer Vaccination Enhances Stem-like Phenotype and Immune Escape, Which Can Be Blocked by Thrombospondin-1 Signaling through CD47 Receptor Protein vol.290, pp.14, 2015, https://doi.org/10.1074/jbc.M114.624965
  7. All-trans retinoic acid suppresses malignant characteristics of CD133-positive thyroid cancer stem cells and induces apoptosis vol.12, pp.8, 2017, https://doi.org/10.1371/journal.pone.0182835