A short-term colorectal cancer sphere culture as a relevant tool for human cancer biology investigation

British Journal of Cancer

Volumn 108, Issue 8, 2013, Pages 1720-1731

  Weiswald, L B ^a,b,h,i   Richon, S ^a   Massonnet, G ^a,c   Guinebretiere J M ^b   Vacher, S ^b   Laurendeau, I ^a,d   Cottu, P ^b,c   Marangoni, E ^c   Nemati, F ^c   Validire, P ^e   Bellet, D ^b,f   Bieche I ^a,b,d   Dangles Marie, V ^a,c,g  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSTITUT CURIE   (France)

^c Centre de Recherche   (France)

^d INSERM   (France)

^e INSTITUT MUTUALISTE MONTSOURIS   (France)

^f Centre National de la Recherche Scientifique   (France)

^g PSL RESEARCH UNIVERSITY   (France)

^h UNIVERSITY OF BRITISH COLUMBIA   (Canada)

ⁱ BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; FLUOROURACIL; IRINOTECAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOIKIS; ARTICLE; CANCER CELL CULTURE; CELL INTERACTION; CHEMOSENSITIVITY; COLORECTAL CANCER; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TUMOR XENOGRAFT;

ANIMALS; CAMPTOTHECIN; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; COLORECTAL NEOPLASMS; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; FLUOROURACIL; HUMANS; MICE; MICE, NUDE; MICE, SCID; MICROSCOPY, CONFOCAL; NEOPLASM TRANSPLANTATION; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; SPHEROIDS, CELLULAR; TRANSPLANTATION, HETEROLOGOUS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84877043848     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.132     Document Type: Article

References (52)

1. Adachi Y, Yamamoto H, Itoh F, Hinoda Y, Okada Y, Imai K (1999) Contribution of matrilysin (MMP-7) to the metastatic pathway of human colorectal cancers. Gut 45(2): 252-258.
2. Bieche I, Parfait B, Le Doussal V, Olivi M, Rio MC, Lidereau R, Vidaud M (2001) Identification of CGA as a novel estrogen receptor-responsive gene in breast cancer: an outstanding candidate marker to predict the response to endocrine therapy. Cancer Res 61(4): 1652-1658.
3. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, Knuechel R, Kirchner T (2001) Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci USA 98(18): 10356-10361.
4. Brabletz T, Spaderna S, Kolb J, Hlubek F, Faller G, Bruns CJ, Jung A, Nentwich J, Duluc I, Domon-Dell C, Kirchner T, Freund JN (2004) Down-regulation of the homeodomain factor Cdx2 in colorectal cancer by collagen type I: an active role for the tumor environment in malignant tumor progression. Cancer Res 64(19): 6973-6977.
5. Briffod M, Hacene K, Le Doussal V (2000) Immunohistochemistry on cell blocks from fine-needle cytopunctures of primary breast carcinomas and lymph node metastases. Mod Pathol 13(8): 841-850.
6. Carlotti F, Bazuine M, Kekarainen T, Seppen J, Pognonec P, Maassen JA, Hoeben RC (2004) Lentiviral vectors efficiently transduce quiescent mature 3T3-L1 adipocytes. Mol Ther 9(2): 209-217.
7. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, Scott EW, Huang EH (2009) Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 69(20): 8208-8215.
8. Chabot GG (1997) Clinical pharmacokinetics of irinotecan. Clin Pharmacokinet 33(4): 245-259.
9. Cheng G, Tse J, Jain RK, Munn LL (2009) Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One 4(2): e4632.
10. Chopra DP, Dombkowski AA, Stemmer PM, Parker GC (2010) Intestinal epithelial cells in vitro. Stem Cells Dev 19(1): 131-142.
11. Dangles-Marie V, Pocard M, Richon S, Weiswald LB, Assayag F, Saulnier P, Judde JG, Janneau JL, Auger N, Validire P, Dutrillaux B, Praz F, Bellet D, Poupon MF (2007) Establishment of human colon cancer cell lines from fresh tumors versus xenografts: comparison of success rate and cell line features. Cancer Res 67(1): 398-407.
12. Daniel VC, Marchionni L, Hierman JS, Rhodes JT, Devereux WL, Rudin CM, Yung R, Parmigiani G, Dorsch M, Peacock CD, Watkins DN (2009) A primary xenograft model of small-cell lung cancer reveals irreversible changes in gene expression imposed by culture in vitro. Cancer Res 69(8): 3364-3373.
13. Debnath J, Brugge JS (2005) Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 5(9): 675-688.
14. Eccles SA, Welch DR (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369(9574): 1742-1757.
15. Emmink BL, Van Houdt WJ, Vries RG, Hoogwater FJ, Govaert KM, Verheem A, Nijkamp MW, Steller EJ, Jimenez CR, Clevers H, Borel Rinkes IH, Kranenburg O (2011) Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan. Gastroenterology 141(1): 269-278.
16. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4(3): 309-324.
17. Gillet JP, Calcagno AM, Varma S, Marino M, Green LJ, Vora MI, Patel C, Orina JN, Eliseeva TA, Singal V, Padmanabhan R, Davidson B, Ganapathi R, Sood AK, Rueda BR, Ambudkar SV, Gottesman MM (2011) Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc Natl Acad Sci USA 108(46): 18708-18713.
18. Gray MJ (2008) Therapeutic targeting of Id2 reduces growth of human colorectal carcinoma in the murine liver. Oncogene 27(57): 7192-7200.
19. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha MS, Boman BM (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(8): 3382-3389.
20. Jacks T, Weinberg RA (2002) Taking the study of cancer cell survival to a new dimension. Cell 111(7): 923-925.
21. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2): 69-90.
22. Jiang T, Collins BJ, Jin N, Watkins DN, Brock MV, Matsui W, Nelkin BD, Ball DW (2009) Achaete-scute complex homologue 1 regulates tumorinitiating capacity in human small cell lung cancer. Cancer Res 69(3): 845-854.
23. Jinesh GG, Choi W, Shah JB, Lee EK, Willis DL, Kamat AM (2013) Blebbishields, the emergency program for cancer stem cells: sphere formation and tumorigenesis after apoptosis. Cell death and differentiation 20(3): 382-395.
24. Johnson JI, Decker S, Zaharevitz D, Rubinstein LV, Venditti JM, Schepartz S, Kalyandrug S, Christian M, Arbuck S, Hollingshead M, Sausville EA (2001) Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br J Cancer 84(10): 1424-1431.
25. Julien S, Merino-Trigo A, Lacroix L, Pocard M, Goere D, Mariani P, Landron S, Bigot L, Nemati F, Dartigues P, Weiswald LB, Lantuas D, Morgand L, Pham E, Gonin P, Dangles-Marie V, Job B, Dessen P, Bruno A, Pierre A, De The H, Soliman H, Nunes M, Lardier G, Calvet L, Demers B, Prevost G, Vrignaud P, Roman-Roman S, Duchamp O, Berthet C (2012) Characterization of a large panel of patient-derived tumor xenografts representing the clinical heterogeneity of human colorectal cancer. Clin Cancer Res 18(19): 5314-5328.
26. Kitamura T, Biyajima K, Aoki M, Oshima M, Taketo MM (2009) Matrix metalloproteinase 7 is required for tumor formation, but dispensable for invasion and fibrosis in SMAD4-deficient intestinal adenocarcinomas. Lab Invest 89(1): 98-105.
27. Kondo J, Endo H, Okuyama H, Ishikawa O, Iishi H, Tsujii M, Ohue M, Inoue M (2011) Retaining cell-cell contact enables preparation and culture of spheroids composed of pure primary cancer cells from colorectal cancer. Proc Natl Acad Sci USA 108(15): 6235-6240.
28. Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98(1): 31-36.
29. Marcato P, Dean CA, Giacomantonio CA, Lee PW (2011) Aldehyde dehydrogenase: its role as a cancer stem cell marker comes down to the specific isoform. Cell Cycle 10(9): 1378-1384.
30. McBain JA, Weese JL, Meisner LF, Wolberg WH, Willson JK (1984) Establishment and characterization of human colorectal cancer cell lines. Cancer Res 44(12 Pt 1): 5813-5821.
31. Merlos-Suárez A, Barriga FM, Jung P, Iglesias M, Céspedes MV, Rossell D, Sevillano M, Hernando-Momblona X, da Silva-Diz V, Muñoz P, Clevers H, Sancho E, Mangues R, Batlle E (2011) The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 8(5): 511-524.
32. Minchinton AI, Tannock IF (2006) Drug penetration in solid tumours. Nat Rev Cancer 6(8): 583-592.
33. O'Brien LE, Zegers MM, Mostov KE (2002) Opinion: building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3(7): 531-537.
34. Ootani A, Li X, Sangiorgi E, Ho QT, Ueno H, Toda S, Sugihara H, Fujimoto K, Weissman IL, Capecchi MR, Kuo CJ (2009) Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat Med 15(6): 701-706.
35. Park JG, Oie HK, Sugarbaker PH, Henslee JG, Chen TR, Johnson BE, Gazdar A (1987) Characteristics of cell lines established from human colorectal carcinoma. Cancer Res 47(24 Pt 1): 6710-6718.
36. Rockman SP, Currie SA, Ciavarella M, Vincan E, Dow C, Thomas RJ, Phillips WA (2001) Id2 is a target of the beta-catenin/T cell factor pathway in colon carcinoma. J Biol Chem 276(48): 45113-45119.
37. Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van den Brink S, Van Houdt WJ, Pronk A, Van Gorp J, Siersema PD, Clevers H (2011) Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141(5): 1762-1772.
38. Schmeichel KL, Bissell MJ (2003) Modeling tissue-specific signaling and organ function in three dimensions. J Cell Sci 116(Pt 12): 2377-2388.
39. Smalley KS, Lioni M, Herlyn M (2006) Life isn't flat: taking cancer biology to the next dimension. In Vitro Cell Dev Biol Anim 42(8-9): 242-247.
40. Sutherland RM (1988) Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 240(4849): 177-184.
41. Takimoto CH, Yee LK, Venzon DJ, Schuler B, Grollman F, Chabuk C, Hamilton JM, Chen AP, Allegra CJ, Grem JL (1999) High inter-and intrapatient variation in 5-fluorouracil plasma concentrations during a prolonged drug infusion. Clin Cancer Res 5(6): 1347-1352.
42. Tentler JJ, Tan AC, Weekes CD, Jimeno A, Leong S, Pitts TM, Arcaroli JJ, Messersmith WA, Eckhardt SG (2012) Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 9(6): 338-350.
43. Vaira V, Fedele G, Pyne S, Fasoli E, Zadra G, Bailey D, Snyder E, Faversani A, Coggi G, Flavin R, Bosari S, Loda M (2010) Preclinical model of organotypic culture for pharmacodynamic profiling of human tumors. Proc Natl Acad Sci USA 107(18): 8352-8356.
44. Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, Perez Alea M, Richel DJ, Stassi G, Medema JP (2008) Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA 105(36): 13427-13432.
45. Voskoglou-Nomikos T, Pater JL, Seymour L (2003) Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin Cancer Res 9(11): 4227-4239.
46. Weiswald LB, Guinebretiere JM, Richon S, Bellet D, Saubamea B, Dangles-Marie V (2010) In situ protein expression in tumour spheres: development of an immunostaining protocol for confocal microscopy. BMC Cancer 10: 106.
47. Weiswald LB, Richon S, Validire P, Briffod M, Lai-Kuen R, Cordelieres FP, Bertrand F, Dargere D, Massonnet G, Marangoni E, Gayet B, Pocard M, Bieche I, Poupon MF, Bellet D, Dangles-Marie V (2009) Newly characterised ex vivo colospheres as a three-dimensional colon cancer cell model of tumour aggressiveness. Br J Cancer 101(3): 473-482.
48. Whitehead RH, Demmler K, Rockman SP, Watson NK (1999) Clonogenic growth of epithelial cells from normal colonic mucosa from both mice and humans. Gastroenterology 117(4): 858-865.
49. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, Double JA, Everitt J, Farningham DA, Glennie MJ, Kelland LR, Robinson V, Stratford IJ, Tozer GM, Watson S, Wedge SR, Eccles SA. Committee of the National Cancer Research I (2010) Guidelines for the welfare and use of animals in cancer research. Br J Cancer 102(11): 1555-1577.
50. Yamada KM, Clark K (2002) Cell biology: survival in three dimensions. Nature 419(6909): 790-791.
51. Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130(4): 601-610.
52. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B (2001) PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7(3): 673-682.