Characterization and propagation of tumor initiating cells derived from colorectal liver metastases: Trials, tribulations and a cautionary note

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  James, Mark I ^a   Howells, Lynne M ^a   Karmokar, Ankur ^a   Higgins, Jennifer A ^a   Greaves, Peter ^a   Cai, Hong ^a   Dennison, Ashley ^b   Metcalfe, Matthew ^b   Garcea, Giuseppe ^b   Lloyd, David M ^b   Berry, David P ^c   Steward, William P ^a   Brown, Karen ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY HOSPITALS OF LEICESTER NHS TRUST   (United Kingdom)

^c UNIVERSITY HOSPITAL OF WALES   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; BEVACIZUMAB; CAPECITABINE; CD133 ANTIGEN; CETUXIMAB; DIPEPTIDYL PEPTIDASE IV; EPITHELIAL CELL ADHESION MOLECULE; FLUOROURACIL; FOLINIC ACID; OXALIPLATIN; CELL ADHESION MOLECULE; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; PROM1 PROTEIN, HUMAN; PROM1 PROTEIN, MOUSE; TUMOR ANTIGEN; TUMOR MARKER;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CHEMOTHERAPY; CANCER STEM CELL; COCULTURE; COLORECTAL CANCER; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER METASTASIS; MAJOR CLINICAL STUDY; MALE; MOUSE; NOD SCID MOUSE; NONHUMAN; SEX DIFFERENCE; TUMOR GROWTH; TUMOR SPHEROID; ANIMAL; CELL LINE; CELL PROLIFERATION; COLORECTAL NEOPLASMS; CYTOLOGY; FLOW CYTOMETRY; LIVER NEOPLASMS; METABOLISM; MIDDLE AGED; MULTICELLULAR SPHEROID; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SECONDARY; TUMOR CELL CULTURE; VERY ELDERLY; XENOGRAFT;

MUS;

AC133 ANTIGEN; AGED; AGED, 80 AND OVER; ALDEHYDE DEHYDROGENASE; ANIMALS; ANTIGENS, CD; ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; CELL ADHESION MOLECULES; CELL LINE; CELL PROLIFERATION; COCULTURE TECHNIQUES; COLORECTAL NEOPLASMS; DIPEPTIDYL PEPTIDASE 4; EPITHELIAL CELL ADHESION MOLECULE; FEMALE; FIBROBLASTS; FLOW CYTOMETRY; GLYCOPROTEINS; HUMANS; LIVER NEOPLASMS; MALE; MICE, INBRED NOD; MICE, SCID; MIDDLE AGED; NEOPLASTIC STEM CELLS; PEPTIDES; SPHEROIDS, CELLULAR; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 84922606067     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117776     Document Type: Article

References (55)

1. UK CR (2014) Available: http://www.cancerresearchuk.org/cancer-info/cancerstats/survival/commoncancers/. Accessed 29/01/2014.
2. Nakamura S, Kino I (1984) Morphogenesis of minute adenomas in familial polyposis coli. J Natl Cancer Inst 73: 41-49. PMID: 6588235
3. Preston SL, Wong WM, Chan AO, Poulsom R, Jeffery R, et al. (2003) Bottom-up histogenesis of colorectal adenomas: origin in the monocryptal adenoma and initial expansion by crypt fission. Cancer Res 63: 3819-3825. PMID: 12839979
4. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, et al. (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115. PMID: 17122771
5. Irollo E, Pirozzi G (2013) CD133: to be or not to be, is this the real question? Am J Transl Res 5: 563-581. PMID: 24093054
6. Grosse-Gehling P, Fargeas CA, Dittfeld C, Garbe Y, Alison MR, et al. (2013) CD133 as a biomarker for putative cancer stem cells in solid tumours: limitations, problems and challenges. J Pathol 229: 355-378. doi: 10.1002/path.4086 PMID: 22899341
7. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, et al. (2008) 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. doi: 10.1172/JCI34401 PMID: 18497886
8. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, et al. (2009) Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69: 3382-3389. doi: 10.1158/0008-5472.CAN-08-4418 PMID: 19336570
9. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, et al. (2009) Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 7: 330-338. doi: 10.1158/1541-7786. MCR-08-0393 PMID: 19276181
10. Gerber JM, Smith BD, Ngwang B, Zhang H, Vala MS, et al. (2012) A clinically relevant population of leukemic CD34(+)CD38(-) cells in acute myeloid leukemia. Blood 119: 3571-3577. doi: 10.1182/blood-2011-06-364182 PMID: 22262762
11. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567. doi: 10.1016/j.stem.2007.08.014 PMID: 18371393
12. Schwitalla S, Fingerle AA, Cammareri P, Nebelsiek T, Goktuna SI, et al. (2013) Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152: 25-38. doi: 10.1016/ j.cell.2012.12.012 PMID: 23273993
13. Hermann PC, Huber SL, Heeschen C (2008) Metastatic cancer stem cells: a new target for anti-cancer therapy? Cell Cycle 7: 188-193. PMID: 18256530
14. Du L, Rao G, Wang H, Li B, Tian W, et al. (2013) CD44-positive cancer stem cells expressing cellular prion protein contribute to metastatic capacity in colorectal cancer. Cancer Res. doi: 10.1158/0008-5472.CAN-13-2440 PMID: 24371232
15. Gao W, Chen L, Ma Z, Du Z, Zhao Z, et al. (2013) Isolation and phenotypic characterization of colorectal cancer stem cells with organ-specific metastatic potential. Gastroenterology 145: 636-646 e635. doi: 10.1053/j.gastro.2013.05.049 PMID: 23747337
16. Irmisch A, Huelsken J (2013) Metastasis: New insights into organ-specific extravasation and metastatic niches. Exp Cell Res. doi: 10.1016/j.yexcr.2013.10.012 PMID: 24512746
17. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, et al. (2010) Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 148: 3-15. doi: 10.1016/j.jbiotec. 2010.01.012 PMID: 20097238
18. Kunz-Schughart L, Freyer J, Hofstaedter F, Ebner R (2004) The Use of 3-D Cultures for High-Throughput Screening: The Multicellular Spheroid Model. Journal of Biomolecular Screening 9: 12. PMID: 15006144
19. Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130: 601-610. PMID: 17719539
20. Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, et al. (2008) Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci U S A 105: 13427-13432. doi: 10.1073/pnas.0805706105 PMID: 18765800
21. Park CY, Tseng D, Weissman IL (2009) Cancer stem cell-directed therapies: recent data from the laboratory and clinic. Mol Ther 17: 219-230. doi: 10.1038/mt.2008.254 PMID: 19066601
22. Guzman ML, Rossi RM, Karnischky L, Li X, Peterson DR, et al. (2005) The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 105: 4163-4169. PMID: 15687234
23. Cammareri P, Lombardo Y, Francipane MG, Bonventre S, Todaro M, et al. (2008) Isolation and culture of colon cancer stem cells. Methods Cell Biol 86: 311-324. doi: 10.1016/S0091-679X(08)00014-9 PMID: 18442654
24. Paduch R, Kandefer-Szerszen M (2011) Expression and activation of proteases in co-cultures. Exp Toxicol Pathol 63: 79-87. doi: 10.1016/j.etp.2009.09.011 PMID: 19836935
25. Vermeulen L, De Sousa EMF, van der Heijden M, Cameron K, de Jong JH, et al. (2010) Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12: 468-476. doi: 10.1038/ncb2048 PMID: 20418870
26. Ye J, Wu D, Wu P, Chen Z, Huang J (2014) The cancer stem cell niche: cross talk between cancer stem cells and their microenvironment. Tumour Biol. PMID: 25549795
27. Waldron J, McCourty A, Lecanu L (2010) Aging differentially affects male and female neural stem cell neurogenic properties. Stem Cells Cloning 3: 119-127. doi: 10.2147/SCCAA.S13035 PMID: 24198517
28. Siegel G, Kluba T, Hermanutz-Klein U, Bieback K, Northoff H, et al. (2013) Phenotype, donor age and gender affect function of human bone marrow-derived mesenchymal stromal cells. BMC Med 11: 146. doi: 10.1186/1741-7015-11-146 PMID: 23758701
29. Herrmann JL, Abarbanell AM, Weil BR, Manukyan MC, Poynter JA, et al. (2010) Gender dimorphisms in progenitor and stem cell function in cardiovascular disease. J Cardiovasc Transl Res 3: 103-113. doi: 10.1007/s12265-009-9149-y PMID: 20376198
30. Mostafa G, Matthews BD, Norton HJ, Kercher KW, Sing RF, et al. (2004) Influence of demographics on colorectal cancer. Am Surg 70: 259-264. PMID: 15055851
31. Chen L, Chang WC, Hung YC, Chang YY, Bao BY, et al. (2013) Androgen Receptor Increases CD133 Expression and Progenitor-Like Population That Associate With Cisplatin Resistance in Endometrial Cancer Cell Line. Reprod Sci. doi: 10.1177/1933719113512533 PMID: 24357638
32. Rousseau A, Ayoubi F, Deveaux C, Charbit B, Delmau C, et al. (2010) Impact of age and gender interaction on circulating endothelial progenitor cells in healthy subjects. Fertil Steril 93: 843-846. doi: 10. 1016/j.fertnstert.2008.10.062 PMID: 19111297
33. Hong SH, Nah HY, Lee YJ, Lee JW, Park JH, et al. (2004) Expression of estrogen receptor-alpha andbeta, glucocorticoid receptor, and progesterone receptor genes in human embryonic stem cells and embryoid bodies. Mol Cells 18: 320-325. PMID: 15650328
34. Li CY, Li BX, Liang Y, Peng RQ, Ding Y, et al. (2009) Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med 7: 56. doi: 10.1186/1479-5876-7-56 PMID: 19583834
35. Reggiani Bonetti L, Migaldi M, Caredda E, Boninsegna A, Ponz De Leon M, et al. (2012) Increased expression of CD133 is a strong predictor of poor outcome in stage I colorectal cancer patients. Scand J Gastroenterol 47: 1211-1217. PMID: 22856425
36. Horst D, Scheel SK, Liebmann S, Neumann J, Maatz S, et al. (2009) The cancer stem cell marker CD133 has high prognostic impact but unknown functional relevance for the metastasis of human colon cancer. J Pathol 219: 427-434. doi: 10.1002/path.2597 PMID: 19621338
37. Chen S, Song X, Chen Z, Li X, Li M, et al. (2013) CD133 expression and the prognosis of colorectal cancer: a systematic review and meta-analysis. PLoS One 8: e56380. doi: 10.1371/journal.pone. 0056380 PMID: 23409180
38. Chirgwin JM (2012) The stem cell niche as a pharmaceutical target for prevention of skeletal metastases. Anticancer Agents Med Chem 12: 187-193. PMID: 22044002
39. Bose D, Zimmerman LJ, Pierobon M, Petricoin E, Tozzi F, et al. (2011) Chemoresistant colorectal cancer cells and cancer stem cells mediate growth and survival of bystander cells. Br J Cancer 105: 1759-1767. doi: 10.1038/bjc.2011.449 PMID: 22045189
40. Borovski T, De Sousa EMF, Vermeulen L, Medema JP (2011) Cancer stem cell niche: the place to be. Cancer Res 71: 634-639. doi: 10.1158/0008-5472.CAN-10-3220 PMID: 21266356
41. Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr H-A, et al. (2012) Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481: 5. doi: 10.1038/481005a PMID: 22222725
42. Saigusa S, Tanaka K, Toiyama Y, Yokoe T, Okugawa Y, et al. (2010) Immunohistochemical features of CD133 expression: association with resistance to chemoradiotherapy in rectal cancer. Oncol Rep 24: 345-350. PMID: 20596619
43. Tamura K, Aoyagi M, Ando N, Ogishima T, Wakimoto H, et al. (2013) Expansion of CD133-positive glioma cells in recurrent de novo glioblastomas after radiotherapy and chemotherapy. J Neurosurg 119: 1145-1155. doi: 10.3171/2013.7.JNS122417 PMID: 23991844
44. Matsuyama M, Wakui M, Monnai M, Mizushima T, Nishime C, et al. (2010) Reduced CD73 expression and its association with altered purine nucleotide metabolism in colorectal cancer cells robustly causing liver metastases. Oncol Lett 1: 431-436. PMID: 22966321
45. Wei B, Han XY, Qi CL, Zhang S, Zheng ZH, et al. (2012) Coaction of spheroid-derived stem-like cells and endothelial progenitor cells promotes development of colon cancer. PLoS One 7: e39069. doi: 10. 1371/journal.pone.0039069 PMID: 22745705
46. Li G, Liu C, Yuan J, Xiao X, Tang N, et al. (2010) CD133(+) single cell-derived progenies of colorectal cancer cell line SW480 with different invasive and metastatic potential. Clin Exp Metastasis 27: 517-527. doi: 10.1007/s10585-010-9341-0 PMID: 20617370
47. Botchkina IL, Rowehl RA, Rivadeneira DE, Karpeh MS Jr, Crawford H, et al. (2009) Phenotypic subpopulations of metastatic colon cancer stem cells: genomic analysis. Cancer Genomics Proteomics 6: 19-29. PMID: 19451087
48. Fan X, Ouyang N, Teng H, Yao H (2011) Isolation and characterization of spheroid cells from the HT29 colon cancer cell line. Int J Colorectal Dis 26: 1279-1285. doi: 10.1007/s00384-011-1248-y PMID: 21670985
49. Masramon L, Vendrell E, Tarafa G, Capella G, Miro R, et al. (2006) Genetic instability and divergence of clonal populations in colon cancer cells in vitro. J Cell Sci 119: 1477-1482. PMID: 16551697
50. Weiswald LB, Richon S, Validire P, Briffod M, Lai-Kuen R, et al. (2009) Newly characterised ex vivo colospheres as a three-dimensional colon cancer cell model of tumour aggressiveness. Br J Cancer 101: 473-482. doi: 10.1038/sj.bjc.6605173 PMID: 19603013
51. Ray S, Langan R, Mullinax J, Koizume T, Xin H-W, et al. (2012) Establishment of Human Ultra-Low Colorectal Cancer Cell Lines Using Spheroids from Fresh Surgical Specimens for In Vitro And In Vivo Studies. Journal of Cancer 3: 11. doi: 10.1093/jscr/2012.3.11 PMID: 24960815
52. Pang R, Law WL, Chu AC, Poon JT, Lam CS, et al. (2010) A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 6: 603-615. doi: 10.1016/j.stem. 2010.04.001 PMID: 20569697
53. Zhang J, Espinoza LA, Kinders RJ, Lawrence SM, Pfister TD, et al. (2012) NANOG modulates stemness in human colorectal cancer. Oncogene. doi: 10.1038/onc.2012.584 PMID: 23246972
54. Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8: 755-768. doi: 10.1038/nrc2499 PMID: 18784658
55. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323. doi: 10.1016/j.stem.2007.06.002 PMID: 18371365