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New ex-ovo colorectal-cancer models from different SdFFF-sorted tumor-initiating cells

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Abstract

Despite effective treatments, relapse of colorectal cancer (CRC) is frequent, in part caused by the existence of tumor-initiating cells (TICs). Different subtypes of TICs, quiescent and activated, coexist in tumors, defining the tumor aggressiveness and therapeutic response. These subtypes have been sorted by hyperlayer sedimentation field-flow fractionation (SdFFF) from WiDr and HCT116 cell lines. On the basis of a new strategy, including TIC SdFFF sorting, 3D Matrigel amplification, and grafting of corresponding TIC colonies on the chick chorioallantoic membrane (CAM), specific tumor matrices could be obtained. If tumors had similar architectural structure with vascularization by the host system, they had different proliferative indices in agreement with their initial quiescent or activated state. Protein analysis also revealed that tumors obtained from a population enriched for “activated” TICs lost “stemness” properties and became invasive. In contrast, tumors obtained from a population enriched for “quiescent” TICs kept their stemness properties and seemed to be less proliferative and invasive. Then, it was possible to produce different kinds of tumor which could be used as selective supports to study carcinogenesis and therapy sensitivity.

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References

  1. Ricci-Vitiani L, Fabrizi E, Palio E, De Maria R (2009) Colon cancer stem cells. J Mol Med 87:1097–1104

    Article  Google Scholar 

  2. 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 93:481–488

    Google Scholar 

  3. Mathonnet M, Perraud A, Christou N, Akil H, Melin C, Battu S, Jauberteau MO, Denizot Y (2014) Hallmarks in colorectal cancer: angiogenesis and cancer stem-like cells. World J Gastroenterol 20:4189–4196

    Article  CAS  Google Scholar 

  4. Karim BO, Huso DL (2013) Mouse models for colorectal cancer. Am J Cancer Res 3:240–250

    Google Scholar 

  5. Balke M, Neumann A, Szuhai K, Agelopoulos K, August C, Gosheger G, Hogendoorn PC, Athanasou NB,H, Hagedorn M (2011) A short-term in vivo model for giant cell tumor of bone. BMC Cancer 11:241. doi:10.1186/1471-2407-11-241

    Article  Google Scholar 

  6. Sun Y, Nelson PS (2012) Molecular pathways: involving microenvironment damage responses in cancer therapy resistance. Clin Cancer Res 18:4019–4025

    Article  CAS  Google Scholar 

  7. Hagedorn M, Zilberberg L, Wilting J, Canron X, Carrabba G, Giussani C, Pluderi M, Bello L, Bikfalvi A (2002) Domain swapping in a COOH-terminal fragment of platelet factor 4 generates potent angiogenesis inhibitors. Cancer Res 62:6884–6890

    CAS  Google Scholar 

  8. Hagedorn M, Javerzat S, Gilges D, Meyre A, de Lafarge B, Eichmann A, Bikfalvi A (2005) Accessing key steps of human tumor progression in vivo by using an avian embryo model. Proc Natl Acad Sci U S A 102:1643–1648

    Article  CAS  Google Scholar 

  9. Balke M, Neumann A, Kersting C, Agelopoulos K, Gebert C, Gosheger G, Buerger H, Hagedorn M (2010) Morphologic characterization of osteosarcoma growth on the chick chorioallantoic membrane. BMC Res Notes 3:58. doi:10.1186/1756-0500-3-58

    Article  Google Scholar 

  10. Dumartin L, Quemener C, Laklai H, Herbert J, Bicknell R, Bousquet C, Pyronnet S, Castronovo V, Schilling MK, Bikfalvi A, Hagedorn M (2010) Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology 138:1595–1606

    Article  CAS  Google Scholar 

  11. Lokman NA, Elder AS, Ricciardelli C, Oehler MK (2012) Chick chorioallantoic membrane (CAM) assay as an in vivo model to study the effect of newly identified molecules on ovarian cancer invasion and metastasis. Int J Mol Sci 13:9959–9970

    Article  CAS  Google Scholar 

  12. Liu M, Scanlon CS, Banerjee R, Russo N, Inglehart RC, Willis AL, Weiss SJ, D'Silva NJ (2013) The histone methyltransferase EZH2 mediates tumor progression on the chick chorioallantoic membrane assay, a novel model of head and neck squamous cell carcinoma. Transl Oncol 36:273–281

    Article  Google Scholar 

  13. Fergelot P, Bernhard JC, Soulet F, Kilarski WW, Léon C, Courtois N, Deminière C, Herbert JM, Antczak P, Falciani F, Rioux-Leclercq N, Patard JJ, Ferrière JM, Ravaud A, Hagedorn M, Bikfalvi A (2013) The experimental renal cell carcinoma model in the chick embryo. Angiogenesis 16:181–194

    Article  Google Scholar 

  14. Subauste MC, Kupriyanova TA, Conn EM, Ardi VC, Quigley JP, Deryugina EI (2009) Evaluation of metastatic and angiogenic potentials of human colon carcinoma cells in chick embryo model systems. Clin Exp Metastasis 26:1033–1047

    Article  Google Scholar 

  15. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, Pickell K, Aguilar J, Lazetic S, Smith-Berdan S, Clarke MF, Hoey T, Lewicki J, Gurney AL (2008) Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 3:e2428. doi:10.1371/ annotation/ 2aa6a20a-e63c-49b6-aeea-aae62435617f

    Article  Google Scholar 

  16. Roy S, Majumdar AP (2012) Cancer stem cells in colorectal cancer: genetic and epigenetic changes. J Stem Cell Res Ther 7:10342. doi:10.4172/2157-7633.S7-006

    Google Scholar 

  17. Moore N, Houghton J, Lyle S (2012) Slow-cycling therapy-resistant cancer cells. Stem Cells Dev 21:1822–1830

    Article  CAS  Google Scholar 

  18. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney AL, Huang EH, Simeone DM, Shelton AA, Parmiani G, Castelli C, Clarke MF (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 104:10158–10163

    Article  CAS  Google Scholar 

  19. Ricci-Vitiani L, Lombardi D, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445:111–115

    Article  CAS  Google Scholar 

  20. Buczacki S, Davies RJ, Winton DJ (2011) Stem cells, quiescence and rectal carcinoma: an unexplored relationship and potential therapeutic target. Br J Cancer 105:1253–1259

    Article  CAS  Google Scholar 

  21. Kleffel S, Schatton T (2013) Tumor dormancy and cancer stem cells: two sides of the same coin? Adv Exp Med Biol 734:145–179

    Article  CAS  Google Scholar 

  22. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445:106–110

    Article  Google Scholar 

  23. Vaiopoulos AG, Kostakis ID, Koutsilieris M, Papavassiliou AG (2012) Colorectal cancer stem cells. Stem Cells 30:363–371

    Article  CAS  Google Scholar 

  24. Cammareri P, Lombardo Y, Francipane MG, Bonventre S, Todaro M, Stassi G (2008) Isolation and culture of colon cancer stem cells. Methods Cell Biol 86:311–324

    Article  CAS  Google Scholar 

  25. Mélin C, Perraud A, Akil H, Jauberteau MO, Cardot P, Mathonnet M, Battu S (2012) Cancer stem cell sorting from colorectal cancer cell lines by sedimentation field flow fractionation. Anal Chem 84:1549–1556

    Article  Google Scholar 

  26. Mélin C, Lacroix A, Lalloué F, Pothier A, Zhang LY, Perraud A, Dalmay C, Lautrette C, Jauberteau MO, Cardot P, Mathonnet M, Battu S (2013) Improved sedimentation field-flow fractionation separation channel for concentrated cellular elution. J Chromatogr A 1302:118–124

    Article  Google Scholar 

  27. Cailleteau C, Micallef L, Lepage C, Cardot PJ, Beneytout JL, Liagre B, Battu S (2010) Investigating the relationship between cell cycle stage and diosgenin-induced megakaryocytic differentiation of HEL cells using sedimentation field-flow fractionation. Anal Bioanal Chem 398:1273–1283

    Article  CAS  Google Scholar 

  28. Ishizu K, Sunose N, Yamazaki K, Tsuruo T, Sadahiro S, Makuuchi H, Yamori T (2007) Development and characterization of a model of liver metastasis using human colon cancer HCT-116 cells. Biol Pharm Bull 30:1779–1783

    Article  CAS  Google Scholar 

  29. Bayrak R, Yenidünya S, Haltas H (2011) Cytokeratin 7 and cytokeratin 20 expression in colorectal adenocarcinomas. Pathol Res Pract 207:156–160

    Article  CAS  Google Scholar 

  30. Han XY, Wei B, Fang JF, Zhang S, Zhang FC, Zhang HB, Lan TY, Lu HQ, Wei HB (2013) Epithelial-mesenchymal transition associates with maintenance of stemness in spheroid-derived stem-like colon cancer cells. PLoS One 8:e73341. doi:10.1371/journal.pone.0073341

    Article  CAS  Google Scholar 

  31. Chu P, Clanton DJ, Snipas TS, Lee J, Mitchell E, Nguyen ML, Hare E, Peach RJ (2009) Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int J Cancer 124:1312–1321

    Article  CAS  Google Scholar 

  32. Dang H, Ding W, Emerson D, Rountree CB (2011) Snail1 induces epithelial-to-mesenchymal transition and tumor initiating stem cell characteristics. BMC Cancer 11:396. doi:10.1186/1471-2407-11-396

    Article  CAS  Google Scholar 

  33. Chen X, Wang Y, Xia H, Wang Q, Jiang X, Lin Z, Ma Y, Yang Y, Hu M (2012) Loss of E-cadherin promotes the growth, invasion and drug resistance of colorectal cancer cells and is associated with liver metastasis. Mol Biol Rep 3:6707–6714

    Article  Google Scholar 

  34. Céspedes MV, Espina C, García-Cabezas MA, Trias M, Boluda A, Gómez del Pulgar MT, Sancho FJ, Nistal M, Lacal JC, Mangues R (2007) Orthotopic microinjection of human colon cancer cells in nude mice induces tumor foci in all clinically relevant metastatic sites. Am J Pathol 170:1077–1085

    Article  Google Scholar 

  35. Bhullar J, Subhas G, Silberberg B, Tilak J, Andrus L, Decker M, Mittal VK (2011) A novel nonoperative orthotopic colorectal cancer murine model using electrocoagulation. J Am Coll Surg 213:54–60

    Article  Google Scholar 

  36. Sadanandam A, Lyssiotis CA, Homicsko K, Collisson EA, Gibb WJ, Wullschleger S, Ostos LC, Lannon WA, Grotzinger C, Del Rio M, Lhermitte B, Olshen AB, Wiedenmann B, Cantley LC, Gray JW, Hanahan D (2013) A colorectal cancer classification system that associates cellular phenotype and responses to therapy. Nat Med 19:619–625

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr J. Cook-Moreau and Dr C. Wilson for corrections in the preparation of this manuscript. The expenses of this work were defrayed in part by the Ministère de l’Education Nationale, de la Recherche et de la Technologie, the Conseil Régional du Limousin, the Ligue contre le Cancer (Comité du Limousin), and the Comité d’Orientation de la Recherche sur le Cancer (CORC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interests.

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    Authors and Affiliations

    1. Université de Limoges, Laboratoire EA 3842, Homéostasie cellulaire et Pathologies, Faculté de Médecine et de Pharmacie, 2 rue du Dr Marcland, 87025, Limoges cedex, France

      Carole Mélin, Aurélie Perraud, Niki Christou, Romain Bibes, Marie-Odile Jauberteau & Muriel Mathonnet

    2. Université de Limoges, Institut Fédératif de Recherche 145 GEIST « Génomique, Environnement, Immunité, Santé et Thérapeutiques », 2 rue du Dr Marcland, 87025, Limoges cedex, France

      Carole Mélin, Aurélie Perraud, Niki Christou, Romain Bibes, Philippe Cardot, Marie-Odile Jauberteau, Serge Battu & Muriel Mathonnet

    3. CHU de Limoges, Service de chirurgie digestive générale et endocrinienne, 2 rue Martin Luther King, 87042, Limoges cedex, France

      Aurélie Perraud, Niki Christou & Muriel Mathonnet

    4. Université de Limoges, Laboratoire de Chimie Analytique, EA 3842, “Homéostasie Cellulaire et Pathologies”, Faculté de Médecine et de Pharmacie, 2 rue du Docteur Marcland, 87025, Limoges Cedex, France

      Philippe Cardot & Serge Battu

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    1. Carole Mélin
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    Correspondence to Serge Battu.

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    Carole Mélin, Aurélie Perraud, Serge Battu and Muriel Mathonnet contributed equally to this work.

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    Mélin, C., Perraud, A., Christou, N. et al. New ex-ovo colorectal-cancer models from different SdFFF-sorted tumor-initiating cells. Anal Bioanal Chem 407, 8433–8443 (2015). https://doi.org/10.1007/s00216-015-9029-z

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    • DOI: https://doi.org/10.1007/s00216-015-9029-z

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