Vasculature analysis of patient derived tumor xenografts using species-specific PCR assays: Evidence of tumor endothelial cells and atypical VEGFA-VEGFR1/2 signalings

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Bieche, Ivan ^a,b   Vacher, Sophie ^a   Vallerand, David ^c,d   Richon, Sophie ^e,f   Hatem, Rana ^a   De Plater, Ludmilla ^c   Dahmani, Ahmed ^c   Némati, Fariba ^c   Angevin, Eric ^g   Marangoni, Elisabetta ^c   Roman Roman, Sergio ^c   Decaudin, Didier ^a,c   Dangles Marie, Virginie ^a,c,h  

^a INSTITUT CURIE   (France)

^b INSERM   (France)

^c Département de Recherche Translationnelle Laboratoire d'Investigation Préclinique   (France)

^d Roche   (France)

^e Faculte de Pharmacie   (France)

^f INSTITUT CURIE   (France)

^g INSTITUT GUSTAVE ROUSSY   (France)

^h UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Endothelial markers; Patient derived xenografts; Species specific PCR assays; Tumor vasculature; VEGFA VEGFR1 2 signalings

Indexed keywords

BEVACIZUMAB; CD31 ANTIGEN; ENDOGLIN; MESSENGER RNA; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CLASSIFICATION; COLORECTAL CANCER; CONTROLLED STUDY; CUTANEOUS MELANOMA; DRUG RESPONSE; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GLIOBLASTOMA; HOUSEKEEPING GENE; HUMAN; HUMAN TISSUE; KIDNEY CANCER; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MOUSE; NONHUMAN; OVARY CANCER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TISSUE SPECIFICITY; TUMOR CELL; TUMOR ENDOTHELIAL CELL; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; AUTOCRINE EFFECT; BREAST CARCINOMA; CANCER CHEMOTHERAPY; CD105 GENE; CD31 GENE; CELL TRANSDIFFERENTIATION; COLORECTAL CARCINOMA; FEMALE; GENE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; KIDNEY CARCINOMA; MELANOMA SKIN CANCER; NON SMALL CELL LUNG CANCER; OVARY CARCINOMA; REAL TIME POLYMERASE CHAIN REACTION; SMALL CELL CARCINOMA; TBP GENE; VEGFA GENE; VEGFR1 GENE; VEGFR2 GENE;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; NEOPLASMS, EXPERIMENTAL; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899089584     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-178     Document Type: Article

References (33)

1. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 2008, 8:579-591. 10.1038/nrc2403, 18596824.
2. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 2005, 23:1011-1027.
3. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 2006, 7:359-371. 10.1038/nrm1911, 16633338.
4. Ping YF, Bian XW. Consice review: Contribution of cancer stem cells to neovascularization. Stem Cells 2011, 29:888-894. 10.1002/stem.650, 21557392.
5. Knizetova P, Ehrmann J, Hlobilkova A, Vancova I, Kalita O, Kolar Z, Bartek J. Autocrine regulation of glioblastoma cell cycle progression, viability and radioresistance through the VEGF-VEGFR2 (KDR) interplay. Cell Cycle 2008, 7:2553-2561. 10.4161/cc.7.16.6442, 18719373.
6. Lichtenberger BM, Tan PK, Niederleithner H, Ferrara N, Petzelbauer P, Sibilia M. Autocrine VEGF signaling synergizes with EGFR in tumor cells to promote epithelial cancer development. Cell 2010, 140:268-279. 10.1016/j.cell.2009.12.046, 20141840.
7. Hamerlik P, Lathia JD, Rasmussen R, Wu Q, Bartkova J, Lee M, Moudry P, Bartek J, Fischer W, Lukas J, Rich JN, Bartek J. Autocrine VEGF-VEGFR2-Neuropilin-1 signaling promotes glioma stem-like cell viability and tumor growth. J Exp Med 2012, 209:507-520. 10.1084/jem.20111424, 3302235, 22393126.
8. Tentler JJ, Tan AC, Weekes CD, Jimeno A, Leong S, Pitts TM, Arcaroli JJ, Messersmith WA, Eckhardt SG. Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 2012, 9:338-350. 10.1038/nrclinonc.2012.61, 3928688, 22508028.
9. Bieche I, Onody P, Laurendeau I, Olivi M, Vidaud D, Lidereau R, Vidaud M. Real-time reverse transcription-PCR assay for future management of ERBB2-based clinical applications. Clin Chem 1999, 45:1148-1156.
10. Baird SM, Beattie GM, Lannom RA, Lipsick JS, Jensen FC, Kaplan NO. Induction of lymphoma in antigenically stimulated athymic mice. Cancer Res 1982, 42:198-206.
11. Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies. Cancer Res 2000, 60:1388-1393.
12. Fukumura D, Xavier R, Sugiura T, Chen Y, Park EC, Lu N, Selig M, Nielsen G, Taksir T, Jain RK, Seed B. Tumor induction of VEGF promoter activity in stromal cells. Cell 1998, 94:715-725. 10.1016/S0092-8674(00)81731-6, 9753319.
13. Liang WC, Wu X, Peale FV, Lee CV, Meng YG, Gutierrez J, Fu L, Malik AK, Gerber HP, Ferrara N, Fuh G. Cross-species vascular endothelial growth factor (VEGF)-blocking antibodies completely inhibit the growth of human tumor xenografts and measure the contribution of stromal VEGF. J Biol Chem 2006, 281:951-961. 10.1074/jbc.M508199200, 16278208.
14. Hendrix MJ, Seftor EA, Hess AR, Seftor RE. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat Rev Cancer 2003, 3:411-421. 10.1038/nrc1092, 12778131.
15. Alvero AB, Fu HH, Holmberg J, Visintin I, Mor L, Marquina CC, Oidtman J, Silasi DA, Mor G. Stem-like ovarian cancer cells can serve as tumor vascular progenitors. Stem Cells 2009, 27:2405-2413. 10.1002/stem.191, 2783765, 19658191.
16. Bussolati B, Bruno S, Grange C, Ferrando U, Camussi G. Identification of a tumor-initiating stem cell population in human renal carcinomas. Faseb J 2008, 22:3696-3705. 10.1096/fj.08-102590, 18614581.
17. Bussolati B, Grange C, Sapino A, Camussi G. Endothelial cell differentiation of human breast tumour stem/progenitor cells. J Cell Mol Med 2009, 13:309-319. 10.1111/j.1582-4934.2008.00338.x, 3087118, 18410528.
18. Hardee ME, Zagzag D. Mechanisms of Glioma-Associated Neovascularization. Am J Pathol 2012, 181:1126-1141. 10.1016/j.ajpath.2012.06.030, 3463636, 22858156.
19. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM, De Maria R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010, 468:824-828. 10.1038/nature09557, 21102434.
20. Soda Y, Marumoto T, Friedmann-Morvinski D, Soda M, Liu F, Michiue H, Pastorino S, Yang M, Hoffman RM, Kesari S, Verma IM. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci U S A 2011, 108:4274-4280. 10.1073/pnas.1016030108, 3060261, 21262804.
21. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010, 468:829-833. 10.1038/nature09624, 21102433.
22. Ghanekar A, Ahmed S, Chen K, Adeyi O. Endothelial cells do not arise from tumor-initiating cells in human hepatocellular carcinoma. BMC Cancer 2013, 13:485. 10.1186/1471-2407-13-485, 3856592, 24138671.
23. 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 Thé H, Soliman H, Nunes M, Lardier G, Calvet L, Demers B, Prevost G, Vrignaud P, Roman-Roman S, Duchamp O, et al. Characterization of a large panel of patient-derived tumor xenografts representing the clinical heterogeneity of human colorectal cancer. Clin Cancer Res 2012, 18:5314-5328. 10.1158/1078-0432.CCR-12-0372, 22825584.
24. Reyal F, Guyader C, Decraene C, Lucchesi C, Auger N, Assayag F, De Plater L, Gentien D, Poupon MF, Cottu P, De Cremoux P, Gestraud P, Vincent-Salomon A, Fontaine JJ, Roman-Roman S, Delattre O, Decaudin D, Marangoni E. Molecular profiling of patient-derived breast cancer xenografts. Breast Cancer Res 2012, 14:R11. 10.1186/bcr3095, 3496128, 22247967.
25. Fonsatti E, Altomonte M, Nicotra MR, Natali PG, Maio M. Endoglin (CD105): a powerful therapeutic target on tumor-associated angiogenetic blood vessels. Oncogene 2003, 22:6557-6563. 10.1038/sj.onc.1206813, 14528280.
26. Angevin E, Glukhova L, Pavon C, Chassevent A, Terrier-Lacombe MJ, Goguel AF, Bougaran J, Ardouin P, Court BH, Perrin JL, Vallancien G, Triebel F, Escudier B. Human renal cell carcinoma xenografts in SCID mice: tumorigenicity correlates with a poor clinical prognosis. Lab Invest 1999, 79:879-888.
27. Cottu P, Marangoni E, Assayag F, de Cremoux P, Vincent-Salomon A, Guyader C, de Plater L, Elbaz C, Karboul N, Fontaine JJ, Chateau-Joubert S, Boudou-Rouquette P, Alran S, Dangles-Marie V, Gentien D, Poupon MF, Decaudin D. Modeling of response to endocrine therapy in a panel of human luminal breast cancer xenografts. Breast Cancer Res Treat 2012, 133:595-606. 10.1007/s10549-011-1815-5, 22002565.
28. de Plater L, Lauge A, Guyader C, Poupon MF, Assayag F, de Cremoux P, Vincent-Salomon A, Stoppa-Lyonnet D, Sigal-Zafrani B, Fontaine JJ, Brough R, Lord CJ, Ashworth A, Cottu P, Decaudin D, Marangoni E. Establishment and characterisation of a new breast cancer xenograft obtained from a woman carrying a germline BRCA2 mutation. Br J Cancer 2010, 103:1192-1200. 10.1038/sj.bjc.6605900, 2967069, 20877358.
29. Leuraud P, Taillandier L, Medioni J, Aguirre-Cruz L, Criniere E, Marie Y, Kujas M, Golmard JL, Duprez A, Delattre JY, Sanson M, Poupon MF. Distinct responses of xenografted gliomas to different alkylating agents are related to histology and genetic alterations. Cancer Res 2004, 64:4648-4653. 10.1158/0008-5472.CAN-03-3429, 15231677.
30. Nemati F, Bras-Goncalves R, Fontaine JJ, de Pinieux G, De Cremoux P, Chapelier A, Daniel C, Laurent-Puig P, Livartowski A, Judde JG, Bordier V, Poupon MF, Decaudin D. Preclinical assessment of cisplatin-based therapy versus docetaxel-based therapy on a panel of human non-small-cell lung cancer xenografts. Anticancer Drugs 2009, 20:932-940. 10.1097/CAD.0b013e32833009cc, 19741504.
31. Nemati F, Daniel C, Arvelo F, Legrier ME, Froget B, Livartowski A, Assayag F, Bourgeois Y, Poupon MF, Decaudin D. Clinical relevance of human cancer xenografts as a tool for preclinical assessment: example of in-vivo evaluation of topotecan-based chemotherapy in a panel of human small-cell lung cancer xenografts. Anticancer Drugs 2010, 21:25-32. 10.1097/CAD.0b013e3283300a29, 19823076.
32. 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. Guidelines for the welfare and use of animals in cancer research. Br J Cancer 2010, 102:1555-1577. 10.1038/sj.bjc.6605642, 2883160, 20502460.
33. Bieche I, Parfait B, Le Doussal V, Olivi M, Rio MC, Lidereau R, Vidaud M. 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 2001, 61:1652-1658.