Tumor grafts derived from patients with head and neck squamous carcinoma authentically maintain the molecular and histologic characteristics of human cancers

Journal of Translational Medicine

Volumn 11, Issue 1, 2013, Pages

  Peng, Shaohua ^a   Creighton, Chad J ^a,b   Zhang, Yiqun ^b   Sen, Banibrata ^a   Mazumdar, Tuhina ^a   Myers, Jeffery N ^a,d   Woolfson, Adrian ^c   Lorenzi, Matthew V ^c   Bell, Diana ^a   Williams, Michelle D ^a   Johnson, Faye M ^a,d  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

Gene expression; Head and neck cancer; Patient derived xenograft; Translational animal models

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GRAFT; CANCER GROWTH; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE EXPRESSION; GROWTH RATE; HEAD AND NECK CARCINOMA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; STROMA CELL; TISSUE CHARACTERIZATION; TUMOR ENGRAFTMENT; TUMOR XENOGRAFT;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; JANUS KINASES; MICE; PROTEIN KINASE INHIBITORS; SRC-FAMILY KINASES; STROMAL CELLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84883114466     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-11-198     Document Type: Article

References (49)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012, 62:10-29. 10.3322/caac.20138, 22237781.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90. 10.3322/caac.20107, 21296855.
3. Smith LP, Thomas GR. Animal models for the study of squamous cell carcinoma of the upper aerodigestive tract: a historical perspective with review of their utility and limitations. Part A. Chemically-induced de novo cancer, syngeneic animal models of HNSCC, animal models of transplanted xenogeneic human tumors. Int J Cancer 2006, 118:2111-2122. 10.1002/ijc.21694, 16380986.
4. Thomas GR, Smith LP. Animal models for the study of squamous cell carcinoma of the upper aerodigestive tract: a historical perspective with review of their utility and limitations part B. Transgenic mouse models. Int J Cancer 2006, 118:2379-2380. 10.1002/ijc.21695, 16380988.
5. Caulin C, Nguyen T, Longley MA, Zhou Z, Wang XJ, Roop DR. Inducible activation of oncogenic K-ras results in tumor formation in the oral cavity. Cancer Res 2004, 64:5054-5058. 10.1158/0008-5472.CAN-04-1488, 15289303.
6. Raimondi AR, Vitale-Cross L, Amornphimoltham P, Gutkind JS, Molinolo A. Rapid development of salivary gland carcinomas upon conditional expression of K-ras driven by the cytokeratin 5 promoter. Am J Pathol 2006, 168:1654-1665. 10.2353/ajpath.2006.050847, 1606594, 16651631.
7. Moral M, Segrelles C, Lara MF, Martinez-Cruz AB, Lorz C, Santos M, Garcia-Escudero R, Lu J, Kiguchi K, Buitrago A, et al. Akt activation synergizes with Trp53 loss in oral epithelium to produce a novel mouse model for head and neck squamous cell carcinoma. Cancer Res 2009, 69:1099-1108. 2914485, 19176372.
8. Myers JN, Holsinger FC, Jasser SA, Bekele BN, Fidler IJ. An orthotopic nude mouse model of oral tongue squamous cell carcinoma. Clin Cancer Res 2002, 8:293-298.
9. Chung CH, Parker JS, Karaca G, Wu J, Funkhouser WK, Moore D, Butterfoss D, Xiang D, Zanation A, Yin X, et al. Molecular classification of head and neck squamous cell carcinomas using patterns of gene expression. Cancer Cell 2004, 5:489-500. 10.1016/S1535-6108(04)00112-6, 15144956.
10. Cutz JC, Guan J, Bayani J, Yoshimoto M, Xue H, Sutcliffe M, English J, Flint J, LeRiche J, Yee J, et al. Establishment in severe combined immunodeficiency mice of subrenal capsule xenografts and transplantable tumor lines from a variety of primary human lung cancers: potential models for studying tumor progression-related changes. Clin Cancer Res 2006, 12:4043-4054. 10.1158/1078-0432.CCR-06-0252, 16818704.
11. Anderson TM, Hess SD, Egilmez NK, Nwogu CE, Lenox JM, Bankert RB. Comparison of human lung cancer/SCID mouse tumor xenografts and cell culture growth with patient clinical outcomes. J Cancer Res Clin Oncol 2003, 129:565-568. 10.1007/s00432-003-0473-3, 12923636.
12. John T, Kohler D, Pintilie M, Yanagawa N, Pham NA, Li M, Panchal D, Hui F, Meng F, Shepherd FA, Tsao MS. The ability to form primary tumor xenografts is predictive of increased risk of disease recurrence in early-stage non-small cell lung cancer. Clin Cancer Res 2011, 17:134-141. 10.1158/1078-0432.CCR-10-2224, 21081655.
13. Monsma DJ, Monks NR, Cherba DM, Dylewski D, Eugster E, Jahn H, Srikanth S, Scott SB, Richardson PJ, Everts RE, et al. Genomic characterization of explant tumorgraft models derived from fresh patient tumor tissue. J Transl Med 2012, 10:125. 10.1186/1479-5876-10-125, 3439334, 22709571.
14. Bertotti A, Migliardi G, Galimi F, Sassi F, Torti D, Isella C, Cora D, Nicolantonio FD, Buscarino MCP, et al. A molecularly annotated platform of patient-derived xenografts (" Xenopatients") identifies HER2 as an effective therapeutic target in Cetuximab-Resistant colorectal cancer. Cancer Discovery 2011, 1:508-523. 10.1158/2159-8290.CD-11-0109, 22586653.
15. Julien S, Merino-Trigo A, Lacroix L, Pocard M, Goere D, Mariani P, Landron S, Bigot L, Nemati F, Dartigues P, 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.
16. Dong X, Guan J, English JC, Flint J, Yee J, Evans K, Murray N, Macaulay C, Ng RT, Gout PW, et al. Patient-derived first generation xenografts of non-small cell lung cancers: promising tools for predicting drug responses for personalized chemotherapy. Clin Cancer Res 2010, 16:1442-1451. 10.1158/1078-0432.CCR-09-2878, 20179238.
17. Reyal F, Guyader C, Decraene C, Lucchesi C, Auger N, Assayag F, De Plater L, Gentien D, Poupon MF, Cottu P, et al. Molecular profiling of patient-derived breast cancer xenografts. Breast Cancer Res 2012, 14:R11. 10.1186/bcr3095, 3496128, 22247967.
18. Fichtner I, Rolff J, Soong R, Hoffmann J, Hammer S, Sommer A, Becker M, Merk J. Establishment of patient-derived non-small cell lung cancer xenografts as models for the identification of predictive biomarkers. Clin Cancer Res 2008, 14:6456-6468. 10.1158/1078-0432.CCR-08-0138, 18927285.
19. Souza GR, Molina JR, Raphael RM, Ozawa MG, Stark DJ, Levin CS, Bronk LF, Ananta JS, Mandelin J, Georgescu MM, et al. Three-dimensional tissue culture based on magnetic cell levitation. Nature Nanotechnol 2010, 5:291-296.
20. Johnson FM, Saigal B, Tran H, Donato NJ. Abrogation of signal transducer and activator of transcription 3 reactivation after Src kinase inhibition results in synergistic antitumor effects. Clin Cancer Res 2007, 13:4233-4244. 10.1158/1078-0432.CCR-06-2981, 17634553.
21. Chaw SY, Majeed AA, Dalley AJ, Chan A, Stein S, Farah CS. Epithelial to mesenchymal transition (EMT) biomarkers-E-cadherin, beta-catenin, APC and Vimentin-in oral squamous cell carcinogenesis and transformation. Oral Oncol 2012, 48:997-1006. 10.1016/j.oraloncology.2012.05.011, 22704062.
22. Konig F, Krekeler G, Honig JF, Cordon-Cardo C, Fischer G, Korabiowska M. Relation between human papillomavirus positivity and p16 expression in head and neck carcinomas-a tissue microarray study. Anticancer Res 2007, 27:283-288.
23. Chen C, Mendez E, Houck J, Fan W, Lohavanichbutr P, Doody D, Yueh B, Futran ND, Upton M, Farwell DG, et al. Gene expression profiling identifies genes predictive of oral squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2008, 17:2152-2162. 10.1158/1055-9965.EPI-07-2893, 2575803, 18669583.
24. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95:14863-14868. 10.1073/pnas.95.25.14863, 24541, 9843981.
25. Saldanha AJ. Java Treeview-extensible visualization of microarray data. Bioinformatics 2004, 20:3246-3248. 10.1093/bioinformatics/bth349, 15180930.
26. Sen B, Peng S, Woods DM, Wistuba I, Bell D, El-Naggar AK, Lai SY, Johnson FM. STAT5A-mediated SOCS2 expression regulates Jak2 and STAT3 activity following c-Src inhibition in head and neck squamous carcinoma. Clin Cancer Res 2012, 18:127-139. 10.1158/1078-0432.CCR-11-1889, 3251692, 22090359.
27. Saintigny P, Peng S, Zhang L, Sen B, Wistuba II, Lippman SM, Girard L, Minna JD, Heymach JV, Johnson FM. Global evaluation of Eph receptors and ephrins in lung adenocarcinomas identifies EphA4 as an inhibitor of cell migration and invasion. Mol Cancer Ther 2012, 11:2021-2032. 10.1158/1535-7163.MCT-12-0030, 3438283, 22807579.
28. Dutsch-Wicherek M, Lazar A, Tomaszewska R, Kazmierczak W, Wicherek L. Analysis of metallothionein and vimentin immunoreactivity in pharyngeal squamous cell carcinoma and its microenvironment. Cell Tissue Res 2013, 352:341-349. 10.1007/s00441-013-1566-1, 3637648, 23397427.
29. DeRose YS, Wang G, Lin YC, Bernard PS, Buys SS, Ebbert MT, Factor R, Matsen C, Milash BA, Nelson E, et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat Med 2011, 17:1514-1520. 10.1038/nm.2454, 3553601, 22019887.
30. Braakhuis BJ, Sneeuwloper G, Snow GB. The potential of the nude mouse xenograft model for the study of head and neck cancer. Arch Otorhinolaryngol 1984, 239:69-79. 10.1007/BF00454264, 6691837.
31. Garrido-Laguna I, Uson M, Rajeshkumar NV, Tan AC, De Oliveira E, Karikari C, Villaroel MC, Salomon A, Taylor G, Sharma R, et al. Tumor engraftment in nude mice and enrichment in stroma- related gene pathways predict poor survival and resistance to gemcitabine in patients with pancreatic cancer. Clin Cancer Res 2011, 17:5793-5800. 10.1158/1078-0432.CCR-11-0341, 3210576, 21742805.
32. Giovanella BC, Vardeman DM, Williams LJ, Taylor DJ, De Ipolyi PD, Greeff PJ, Stehlin JS, Ullrich A, Cailleau R, Slamon DJ, et al. Heterotransplantation of human breast carcinomas in nude mice. Correlation between successful heterotransplants, poor prognosis and amplification of the HER-2/neu oncogene. Int J Cancer 1991, 47:66-71. 10.1002/ijc.2910470113, 1985881.
33. Braakhuis BJ, Laarman DA, Nauta JJ, Van Walsum M, Van Dongen GA, Snow GB. Transplantability of human head and neck squamous cell carcinomas in athymic nude mice. Arch Otolaryngol Head Neck Surg 1989, 115:1076-1078. 10.1001/archotol.1989.01860330066018, 2765223.
34. Robbins KT, Rosenberg W, Weiss B, Varki NM. Growth characteristics of human laryngeal carcinoma in athymic mice. J Otolaryngol 1991, 20:117-122.
35. Wennerberg J. Changes in growth pattern of human squamous-cell carcinomas of the head and neck during serial passages in nude mice. Int J Cancer 1984, 33:245-250. 10.1002/ijc.2910330213, 6693202.
36. Wennerberg J, Trope C, Biorklund A. Heterotransplantation of human head and neck tumours into nude mice. Acta Otolaryngol 1983, 95:183-190. 10.3109/00016488309130933, 6829300.
37. Zatterstrom UK, Wennerberg J, Attewell R, Ask A. Squamous cell carcinoma of the head and neck heterotransplanted to nude mice: Take rate in relation to patient survival. Cancer 1990, 66:145-151. 10.1002/1097-0142(19900701)66:1<145::AID-CNCR2820660126>3.0.CO;2-0, 2354400.
38. Zatterstrom UK, Wennerberg J. Growth of xenografted head and neck cancer in nude mice pre-treated with whole body irradiation. Acta Otolaryngol 1991, 111:1170-1177.
39. Zatterstrom UK, Kallen A, Wennerberg J. Cell cycle time, growth fraction and cell loss in xenografted head and neck cancer. In Vivo 1991, 5:137-142.
40. Zatterstrom UK, Braakhuis BJ, Wennerberg J, Van Dongen GA, Attewell R, Nauta JJ, Laarman DA, Ask A. Growth of xenografted squamous cell carcinoma of the head and neck-possible correlation with patient survival. APMIS 1992, 100:976-980. 10.1111/j.1699-0463.1992.tb04028.x, 1472366.
41. Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet 2003, 33:49-54.
42. Efferth T, Koomagi R, Mattern J, Volm M. Expression profile of proteins involved in the xenotransplantability of non-small cell lung cancers into athymic nude mice. Int J Oncol 2002, 20:391-395.
43. Simpson-Abelson MR, Sonnenberg GF, Takita H, Yokota SJ, Conway TF, Kelleher RJ, Shultz LD, Barcos M, Bankert RB. Long-term engraftment and expansion of tumor-derived memory T cells following the implantation of non-disrupted pieces of human lung tumor into NOD-scid IL2Rgamma(null) mice. J Immunol 2008, 180:7009-7018.
44. Bergamaschi A, Hjortland GO, Triulzi T, Sorlie T, Johnsen H, Ree AH, Russnes HG, Tronnes S, Maelandsmo GM, Fodstad O, et al. Molecular profiling and characterization of luminal-like and basal-like in vivo breast cancer xenograft models. Mol Oncol 2009, 3:469-482. 10.1016/j.molonc.2009.07.003, 19713161.
45. Daniel VC, Marchionni L, Hierman JS, Rhodes JT, Devereux WL, Rudin CM, Yung R, Parmigiani G, Dorsch M, Peacock CD, Watkins DN. A primary xenograft model of small-cell lung cancer reveals irreversible changes in gene expression imposed by culture in vitro. Cancer Res 2009, 69:3364-3373. 10.1158/0008-5472.CAN-08-4210, 2821899, 19351829.
46. Hidalgo M, Bruckheimer E, Rajeshkumar NV, Garrido-Laguna I, De Oliveira E, Rubio-Viqueira B, Strawn S, Wick MJ, Martell J, Sidransky D. A pilot clinical study of treatment guided by personalized tumorgrafts in patients with advanced cancer. Mol Cancer Ther 2011, 10:1311-1316. 10.1158/1535-7163.MCT-11-0233, 21673092.
47. Ito M, Hiramatsu H, Kobayashi K, Suzue K, Kawahata M, Hioki K, Ueyama Y, Koyanagi Y, Sugamura K, Tsuji K, et al. NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 2002, 100:3175-3182. 10.1182/blood-2001-12-0207, 12384415.
48. Kim MP, Evans DB, Wang H, Abbruzzese JL, Fleming JB, Gallick GE. Generation of orthotopic and heterotopic human pancreatic cancer xenografts in immunodeficient mice. Nat Protoc 2009, 4:1670-1680. 10.1038/nprot.2009.171, 19876027.
49. Bankert RB, Balu-Iyer SV, Odunsi K, Shultz LD, Kelleher RJ, Barnas JL, Simpson-Abelson M, Parsons R, Yokota SJ. Humanized mouse model of ovarian cancer recapitulates patient solid tumor progression, ascites formation, and metastasis. PLoS One 2011, 6:e24420. 10.1371/journal.pone.0024420, 3174163, 21935406.