Animal Models of Oral Cancer Metastasis

Chapter

Abstract

Metastasis is a complex, highly coordinated series of events in which cells from a primary tumor invade lymphatic and/or blood vessels and spread to regional lymph nodes and/or distant organs, establishing proliferating tumor deposits. Because this process requires the interaction of tumor cells with many types of normal cells, tissues, and systems of an intact organism, in vitro model systems provide very limited information regarding the biology of metastasis. Therefore, in vivo model systems are needed to further our understanding of the metastatic process. Several major types of murine model systems have been most informative and include those in which tumor cells are implanted into tissues or injected into the blood system. Also useful are autochthonous models, in which tumors with metastatic potential are induced at the primary site, in this case, the oral cavity, through treatment of the oral mucosa with chemical carcinogens or by genetically engineering changes in the expression of oncogenes and tumor suppressor genes in the oral epithelia. This chapter summarizes the progress that has been made in the development of mouse models of metastasis in oral cancer and the contributions of these models to our understanding of the biology of oral cancer metastasis.

Keywords

Migration Lymphoma Adenocarcinoma Sarcoma Assure 

References

  1. Andres AC, Schonenberger CA, Groner B, Hennighausen L, LeMeur M, Gerlinger P (1987) Ha-ras oncogene expression directed by a milk protein gene promoter: tissue specificity, hormonal regulation, and tumor induction in transgenic mice. Proc Natl Acad Sci USA 84:1299–1303PubMedCrossRefGoogle Scholar
  2. Baker SR (1985) An in vivo model for squamous cell carcinoma of the head and neck. Laryngoscope 95:43–56PubMedCrossRefGoogle Scholar
  3. Bibby MC (2004) Orthotopic models of cancer for preclinical drug evaluation: Advantages and disadvantages. Eur J Cancer 40:852–857PubMedCrossRefGoogle Scholar
  4. Braakhuis BJ, Sneeuwloper G, Snow GB (1984) The potential of the nude mouse xenograft model for the study of head and neck cancer. Arch Otorhinolaryngol 239:69–79PubMedCrossRefGoogle Scholar
  5. Caulin C, Nguyen T, Longley MA, Zhou Z, Wang XJ, Roop DR (2004) Inducible activation of oncogenic K-ras results in tumor formation in the oral cavity. Cancer Res 64:5054–5058PubMedCrossRefGoogle Scholar
  6. Caulin C, Nguyen T, Lang GA, Goepfert TM, Brinkley BR, Cai WW, Lozano G, Roop DR (2007) An inducible mouse model for skin cancer reveals distinct roles for gain- and loss-of-function p53 mutations. J Clin Invest 117:1893–1901PubMedCrossRefGoogle Scholar
  7. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805PubMedCrossRefGoogle Scholar
  8. Chang KW, Sarraj S, Lin SC, Tsai PI, Solt D (2000) P53 expression, p53 and Ha-ras mutation and telomerase activation during nitrosamine-mediated hamster pouch carcinogenesis. Carcinogenesis 21:1441–1451PubMedCrossRefGoogle Scholar
  9. Cheng L, Fu J, Tsukamoto A, Hawley RG (1996) Use of green fluorescent protein variants to monitor gene transfer and expression in mammalian cells. Nat Biotechnol 14:606–609PubMedCrossRefGoogle Scholar
  10. Chung CH, Parker JS, Karaca G, Wu J, Funkhouser WK, Moore D, Butterfoss D, Xiang D, Zanation A, Yin X, Shockley WW, Weissler MC, Dressler LG, Shores CG, Yarbrough WG, Perou CM (2004) Molecular classification of head and neck squamous cell carcinomas using patterns of gene expression. Cancer Cell 5:489–500PubMedCrossRefGoogle Scholar
  11. Clark EA, Golub TR, Lander ES, Hynes RO (2000) Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406:532–535PubMedCrossRefGoogle Scholar
  12. Contag CH, Jenkins D, Contag PR, Negrin RS (2000) Use of reporter genes for optical measurements of neoplastic disease in vivo. Neoplasia 2:41–52PubMedCrossRefGoogle Scholar
  13. Craig G (1980) Metastasis from DMBA-induced carcinomas in hamster cheek pouch. In: Hillman K, Hilgard P, Eccles S (eds) Metastasis clinical and experimental aspects, developments in oncology. Martinus Nijhoff, The Hague, pp 50–54Google Scholar
  14. Cui N, Nomura T, Noma H, Yokoo K, Takagi R, Hashimoto S, Okamoto M, Sato M, Yu G, Guo C, Shibahala T (2005) Effect of YM529 on a model of mandibular invasion by oral squamous cell carcinoma in mice. Clin Cancer Res 11:2713–2719PubMedCrossRefGoogle Scholar
  15. Dachi SF, Sanders JE, Urie EM (1967) Effects of dimethyl sulfoxide on dimethylbenzanthracene-induced carcinogenesis in the hamster cheek pouch. Cancer Res 27:1183–1185PubMedGoogle Scholar
  16. Dinesman A, Haughey B, Gates GA, Aufdemorte T, Von Hoff DD (1990) Development of a new in vivo model for head and neck cancer. Otolaryngol Head Neck Surg 103:766–774PubMedGoogle Scholar
  17. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, Bradley A (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215–221PubMedCrossRefGoogle Scholar
  18. Erdem NF, Carlson ER, Gerard DA (2008) Characterization of gene expression profiles of 3 different human oral squamous cell carcinoma cell lines with different invasion and metastatic capacities. J Oral Maxillofac Surg 66:918–927PubMedCrossRefGoogle Scholar
  19. Fidler IJ (1973) Selection of successive tumour lines for metastasis. Nat New Biol 242:148–149PubMedGoogle Scholar
  20. Fidler IJ, Kripke ML (1977) Metastasis results from preexisting variant cells within a malignant tumor. Science 197:893–895PubMedCrossRefGoogle Scholar
  21. Fidler IJ, Wilmanns C, Staroselsky A, Radinsky R, Dong Z, Fan D (1994) Modulation of tumor cell response to chemotherapy by the organ environment. Cancer Metastasis Rev 13:209–222PubMedCrossRefGoogle Scholar
  22. Fiebig HH, Berger DP (1995) Preclinical phase II trials. In: Boven E, Winograd B (eds) The nude mouse in oncology research. CRC Press, Boca Raton, pp 318–335Google Scholar
  23. Fitch KA, Somers KD, Schecter GL (1988) The development of a head and neck tumor model in the nude mouse. In: Proceedings of the 2nd international head and a neck oncology research conference, Kugler Publications, Amsterdam, pp 187–190Google Scholar
  24. Fujino H, Chino T, Imai T (1965) Experimental production of labial and lingual carcinoma by local application of 4-nitroquinoline N-oxide. J Natl Cancer Inst 35:907–918PubMedGoogle Scholar
  25. Fujita K, Kaku T, Sasaki M, Onoe T (1973) Experimental production of lingual carcinomas in hamsters by local application of 9, 10-dimethyl-1, 2-benzanthracene. J Dent Res 52:327–332PubMedGoogle Scholar
  26. Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, Zahurak ML, Daniel RW, Viglione M, Symer DE, Shah KV, Sidransky D (2000) Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 92:709–720PubMedCrossRefGoogle Scholar
  27. Gimenez-Conti IB, Bianchi AB, Stockman SL, Conti CJ, Slaga TJ (1992) Activating mutation of the Ha-ras gene in chemically induced tumors of the hamster cheek pouch. Mol Carcinog 5:259–263PubMedCrossRefGoogle Scholar
  28. Gimenez-Conti IB, LaBate M, Liu F, Osterndorff E (1996) p53 Alterations in chemically induced hamster cheek-pouch lesions. Mol Carcinog 16:197–202PubMedCrossRefGoogle Scholar
  29. Habu S, Fukui H, Shimamura K, Kasai M, Nagai Y, Okumura K, Tamaoki N (1981) In vivo effects of anti-asialo GM1. I. Reduction of NK activity and enhancement of transplanted tumor growth in nude mice. J Immunol 127:34–38PubMedGoogle Scholar
  30. Hart IR, Fidler IJ (1980) Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res 40:2281–2287PubMedGoogle Scholar
  31. Hawkins BL, Heniford BW, Ackermann DM, Leonberger M, Martinez SA, Hendler FJ (1994) 4NQO carcinogenesis: A mouse model of oral cavity squamous cell carcinoma. Head Neck 16:424–432PubMedCrossRefGoogle Scholar
  32. Henson B, Li F, Coatney DD, Carey TE, Mitra RS, Kirkwood KL, D’Silva NJ (2007) An orthotopic floor-of-mouth model for locoregional growth and spread of human squamous cell carcinoma. J Oral Pathol Med 36:363–370PubMedCrossRefGoogle Scholar
  33. Hier MP, Black MJ, Shenouda G, Sadeghi N, Karp SE (1995) A murine model for the immunotherapy of head and neck squamous cell carcinoma. Laryngoscope 105:1077–1080PubMedCrossRefGoogle Scholar
  34. Hill R (2002) Tumour metastasis models. In: Alison M (ed) The cancer handbook. Nature Publishing Group, LondonGoogle Scholar
  35. Hirst DG, Brown JM, Hazlehurst JL (1982) Enhancement of CCNU cytotoxicity by misonidazole: Possible therapeutic gain. Br J Cancer 46:109–116PubMedGoogle Scholar
  36. Hoffman R (2002) Green fluorescent protein imaging of tumour growth, metastasis, and angiogenesis in mouse models. Lancet Oncol 3:546–556PubMedCrossRefGoogle Scholar
  37. Huang X, Godfrey TE, Gooding WE, McCarty KS Jr, Gollin SM (2006) Comprehensive genome and transcriptome analysis of the 11q13 amplicon in human oral cancer and synteny to the 7F5 amplicon in murine oral carcinoma. Genes Chromosomes Cancer 45:1058–1069PubMedCrossRefGoogle Scholar
  38. Husain Z, Fei YB, Roy S, Solt DB, Polverini PJ, Biswas DK (1989) Sequential expression and cooperative interaction of c-Ha-ras and c-erbB genes in in vivo chemical carcinogenesis. Proc Natl Acad Sci USA 86:1264–1268PubMedCrossRefGoogle Scholar
  39. Ide F, Oda H, Nakatsuru Y, Kusama K, Sakashita H, Tanaka K, Ishikawa T (2001) Xeroderma pigmentosum group A gene action as a protection factor against 4-nitroquinoline 1-oxide-induced tongue carcinogenesis. Carcinogenesis 22:567–572PubMedCrossRefGoogle Scholar
  40. Ide F, Kitada M, Sakashita H, Kusama K, Tanaka K, Ishikawa T (2003) p53 Haploinsufficiency profoundly accelerates the onset of tongue tumors in mice lacking the xeroderma pigmentosum group A gene. Am J Pathol 163:1729–1733PubMedGoogle Scholar
  41. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA (1992) Effects of an Rb mutation in the mouse. Nature 359:295–300PubMedCrossRefGoogle Scholar
  42. Ji RC (2006) Lymphatic endothelial cells, tumor lymphangiogenesis and metastasis: New insights into intratumoral and peritumoral lymphatics. Cancer Metastasis Rev 25:677–694PubMedCrossRefGoogle Scholar
  43. Jiang C, Ye D, Qiu W, Zhang X, Zhang Z, He D, Zhang P, Chen W (2007) Response of lymphocyte subsets and cytokines to Shenyang prescription in Sprague-Dawley rats with tongue squamous cell carcinomas induced by 4NQO. BMC Cancer 7:40PubMedCrossRefGoogle Scholar
  44. 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 84:1424–1431PubMedCrossRefGoogle Scholar
  45. Kage T, Mogi M, Katsumata Y, Chino T (1987) Regional lymph node metastasis created by partial excision of carcinomas induced in hamster cheek pouch with 9, 10-dimethyl-1, 2-benzanthracene. J Dent Res 66:1673–1679PubMedGoogle Scholar
  46. Kanojia D, Vaidya MM (2006) 4-Nitroquinoline-1-oxide induced experimental oral carcinogenesis. Oral Oncol 42:655–667PubMedCrossRefGoogle Scholar
  47. Kasai M, Yoneda T, Habu S, Maruyama Y, Okumura K, Tokunaga T (1981) In vivo effect of anti-asialo GM1 antibody on natural killer activity. Nature 291:334–335PubMedCrossRefGoogle Scholar
  48. Kawashiri S, Kumagai S, Kojima K, Harada H, Yamamoto E (1995) Development of a new invasion and metastasis model of human oral squamous cell carcinomas. Eur J Cancer B Oral Oncol 31B:216–221PubMedCrossRefGoogle Scholar
  49. Kawashiri S, Kumagai S, Kojima K, Harada H, Nakagawa K, Yamamoto E (1999) Reproduction of occult metastasis of head and neck cancer in nude mice. Clin Exp Metastasis 17:277–282PubMedCrossRefGoogle Scholar
  50. Kellendonk C, Tronche F, Monaghan AP, Angrand PO, Stewart F, Schutz G (1996) Regulation of Cre recombinase activity by the synthetic steroid RU 486. Nucleic Acids Res 24:1404–1411PubMedCrossRefGoogle Scholar
  51. Khurana D, Martin EA, Kasperbauer JL, O’Malley BW Jr, Salomao DR, Chen L, Strome SE (2001) Characterization of a spontaneously arising murine squamous cell carcinoma (SCC VII) as a prerequisite for head and neck cancer immunotherapy. Head Neck 23:899–906PubMedCrossRefGoogle Scholar
  52. Komatsubara H, Umeda M, Oku N, Komori T (2002) Establishment of in vivo metastasis model of human adenoid cystic carcinoma: Detection of metastasis by PCR with human beta-globin gene. Kobe J Med Sci 48:145–152PubMedGoogle Scholar
  53. Ku TK, Nguyen DC, Karaman M, Gill P, Hacia JG, Crowe DL (2007) Loss of p53 expression correlates with metastatic phenotype and transcriptional profile in a new mouse model of head and neck cancer. Mol Cancer Res 5:351–362PubMedCrossRefGoogle Scholar
  54. Kuo TH, Kubota T, Watanabe M, Furukawa T, Kase S, Tanino H, Saikawa Y, Ishibiki K, Kitajima M, Hoffman RM (1993) Site-specific chemosensitivity of human small-cell lung carcinoma growing orthotopically compared to subcutaneously in SCID mice: The importance of orthotopic models to obtain relevant drug evaluation data. Anticancer Res 13:627–630PubMedGoogle Scholar
  55. Lang GA, Iwakuma T, Suh YA, Liu G, Rao VA, Parant JM, Valentin-Vega YA, Terzian T, Caldwell LC, Strong LC, el Naggar AK, Lozano G (2004) Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 119:861–872PubMedCrossRefGoogle Scholar
  56. Lee TK, Poon RT, Wo JY, Ma S, Guan XY, Myers JN, Altevogt P, Yuen AP (2007) Lupeol suppresses cisplatin-induced nuclear factor-kappaB activation in head and neck squamous cell carcinoma and inhibits local invasion and nodal metastasis in an orthotopic nude mouse model. Cancer Res 67:8800–8809PubMedCrossRefGoogle Scholar
  57. Levij IS, Polliack A, Thorgeirsson T (1967) Correlation of cytologic smear and histologic findings during 9-10 dimethyl 1-2 benzanthracene-induced carcinogenesis in the hamster cheek pouch. Arch Oral Biol 12:859–864PubMedCrossRefGoogle Scholar
  58. Lin WC, Pretlow TP, Pretlow TG, Culp LA (1990) Bacterial lacZ gene as a highly sensitive marker to detect micrometastasis formation during tumor progression. Cancer Res 50:2808–2817PubMedGoogle Scholar
  59. Lou E, Kellman RM, Shillitoe EJ (2002) Effect of herpes simplex virus type-1 on growth of oral cancer in an immunocompetent, orthotopic mouse model. Oral Oncol 38:349–356PubMedCrossRefGoogle Scholar
  60. Lou E, Kellman RM, Hutchison R, Shillitoe EJ (2003) Clinical and pathological features of the murine AT-84 orthotopic model of oral cancer. Oral Dis 9:305–312PubMedCrossRefGoogle Scholar
  61. Lu SL, Herrington H, Reh D, Weber S, Bornstein S, Wang D, Li AG, Tang CF, Siddiqui Y, Nord J, Andersen P, Corless CL, Wang XJ (2006) Loss of transforming growth factor-beta type II receptor promotes metastatic head-and-neck squamous cell carcinoma. Genes Dev 20:1331–1342PubMedCrossRefGoogle Scholar
  62. Maekawa K, Sato H, Furukawa M, Yoshizaki T (2002) Inhibition of cervical lymph node metastasis by marimastat (BB-2516) in an orthotopic oral squamous cell carcinoma implantation model. Clin Exp Metastasis 19:513–518PubMedCrossRefGoogle Scholar
  63. Matsui T, Ota T, Ueda Y, Tanino M, Odashima S (1998) Isolation of a highly metastatic cell line to lymph node in human oral squamous cell carcinoma by orthotopic implantation in nude mice. Oral Oncol 34:253–256PubMedGoogle Scholar
  64. McKaig RG, Baric RS, Olshan AF (1998) Human papillomavirus and head and neck cancer: Epidemiology and molecular biology. Head Neck 20:250–265PubMedCrossRefGoogle Scholar
  65. Melancon MP, Wang Y, Wen X, Bankson JA, Stephens LC, Jasser S, Gelovani JG, Myers JN, Li C (2007) Development of a macromolecular dual-modality MR-optical imaging for sentinel lymph node mapping. Invest Radiol 42:569–578PubMedCrossRefGoogle Scholar
  66. Momose F, Araida T, Negishi A, Ichijo H, Shioda S, Sasaki S (1989) Variant sublines with different metastatic potentials selected in nude mice from human oral squamous cell carcinomas. J Oral Pathol Med 18:391–395PubMedCrossRefGoogle Scholar
  67. Morin JG, Hastings JW (1971) Energy transfer in a bioluminescent system. J Cell Physiol 77:313–318PubMedCrossRefGoogle Scholar
  68. Muller D, Millon R, Lidereau R, Engelmann A, Bronner G, Flesch H, Eber M, Methlin G, Abecassis J (1994) Frequent amplification of 11q13 DNA markers is associated with lymph node involvement in human head and neck squamous cell carcinomas. Eur J Cancer B Oral Oncol 30B:113–120PubMedCrossRefGoogle Scholar
  69. Muscarella P, Knobloch TJ, Ulrich AB, Casto BC, Moniaux N, Wittel UA, Melvin WS, Pour PM, Song H, Gold B, Batra SK, Weghorst CM (2001) Identification and sequencing of the Syrian Golden hamster (Mesocricetus auratus) p16(INK4a) and p15(INK4b) cDNAs and their homozygous gene deletion in cheek pouch and pancreatic tumor cells. Gene 278:235–243PubMedCrossRefGoogle Scholar
  70. Myers JN, Holsinger FC, Jasser SA, Bekele BN, Fidler IJ (2002) An orthotopic nude mouse model of oral tongue squamous cell carcinoma. Clin Cancer Res 8:293–298PubMedGoogle Scholar
  71. Nakagawa H, Wang TC, Zukerberg L, Odze R, Togawa K, May GH, Wilson J, Rustgi AK (1997) The targeting of the cyclin D1 oncogene by an Epstein-Barr virus promoter in transgenic mice causes dysplasia in the tongue, esophagus and forestomach. Oncogene 14:1185–1190PubMedCrossRefGoogle Scholar
  72. Nakajima J, Mogi M, Chino T (1996) Inhibition by streptococcal immunopotentiator OK432 of lymph-node metastasis in hamster cheek-pouch carcinoma with enhancement of tumour necrosis factor-alpha and interleukin-6 in serum. Arch Oral Biol 41:513–516PubMedCrossRefGoogle Scholar
  73. Nomura T, Shibahara T, Katakura A, Matsubara S, Takano N (2007) Establishment of a murine model of bone invasion by oral squamous cell carcinoma. Oral Oncol 43:257–262PubMedCrossRefGoogle Scholar
  74. O’Donnell RK, Kupferman M, Wei SJ, Singhal S, Weber R, O’Malley B, Cheng Y, Putt M, Feldman M, Ziober B, Muschel RJ (2005) Gene expression signature predicts lymphatic metastasis in squamous cell carcinoma of the oral cavity. Oncogene 24:1244–1251PubMedCrossRefGoogle Scholar
  75. O’Malley BW Jr, Cope KA, Johnson CS, Schwartz MR (1997) A new immunocompetent murine model for oral cancer. Arch Otolaryngol Head Neck Surg 123:20–24PubMedGoogle Scholar
  76. Ohne M, Satoh T, Yamada S, Takai H (1985) Experimental tongue carcinoma of rats induced by oral administration of 4-nitroquinoline 1-oxide (4NQO) in drinking water. Oral Surg Oral Med Oral Pathol 59:600–607PubMedCrossRefGoogle Scholar
  77. Olive KP, Tuveson DA, Ruhe ZC, Yin B, Willis NA, Bronson RT, Crowley D, Jacks T (2004) Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell 119:847–860PubMedCrossRefGoogle Scholar
  78. Opitz OG, Harada H, Suliman Y, Rhoades B, Sharpless NE, Kent R, Kopelovich L, Nakagawa H, Rustgi AK (2002) A mouse model of human oral-esophageal cancer. J Clin Invest 110:761–769PubMedGoogle Scholar
  79. Paget S (1889) The distribution of secondary growths in cancer of the breast. Lancet 1:571–573CrossRefGoogle Scholar
  80. Patel A, Miller L, Ahmed K, Ondrey F (2004) NF-Kappa-B downregulation strategies in head and neck cancer treatment. Otolaryngol Head Neck Surg 131:288–295PubMedCrossRefGoogle Scholar
  81. Qiu C, Wu H, He H, Qiu W (2003) A cervical lymph node metastatic model of human tongue carcinoma: Serial and orthotopic transplantation of histologically intact patient specimens in nude mice. J Oral Maxillofac Surg 61:696–700PubMedCrossRefGoogle Scholar
  82. Roepman P, Wessels LF, Kettelarij N, Kemmeren P, Miles AJ, Lijnzaad P, Tilanus MG, Koole R, Hordijk GJ, van der Vliet PC, Reinders MJ, Slootweg PJ, Holstege FC (2005) An expression profile for diagnosis of lymph node metastases from primary head and neck squamous cell carcinomas. Nat Genet 37:182–186PubMedCrossRefGoogle Scholar
  83. Roepman P, de Jager A, Groot Koerkamp MJ, Kummer JA, Slootweg PJ, Holstege FC (2006) Maintenance of head and neck tumor gene expression profiles upon lymph node metastasis. Cancer Res 66:11110–11114PubMedCrossRefGoogle Scholar
  84. Rounbehler RJ, Schneider-Broussard R, Conti CJ, Johnson DG (2001) Myc lacks E2F1’s ability to suppress skin carcinogenesis. Oncogene 20:5341–5349PubMedCrossRefGoogle Scholar
  85. Rubin JS, Qiu L, Etkind P (1995) Amplification of the Int-2 gene in head and neck squamous cell carcinoma. J Laryngol Otol 109:72–76PubMedGoogle Scholar
  86. Ruther U, Garber C, Komitowski D, Muller R, Wagner EF (1987) Deregulated c-fos expression interferes with normal bone development in transgenic mice. Nature 325:412–416PubMedCrossRefGoogle Scholar
  87. Rwomushana JW, Polliack A, Levij IS (1970) Cervical lymph node metastasis of hamster cheek pouch carcinoma induced with DMBA. J Dent Res 49:184PubMedGoogle Scholar
  88. Safour IM, Wood NK, Tsiklakis K, Doemling DB, Joseph G (1984) Incisional biopsy and seeding in hamster cheek pouch carcinoma. J Dent Res 63:1116–1120PubMedGoogle Scholar
  89. Salley JJ (1954) Experimental carcinogenesis in the cheek pouch of the Syrian hamster. J Dent Res 33:253–262PubMedGoogle Scholar
  90. Sano D, Myers JN (2007) Metastasis of squamous cell carcinoma of the oral tongue. Cancer Metastasis Rev 26:645–662PubMedCrossRefGoogle Scholar
  91. Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA (1996) Role of the INK4a locus in tumor suppression and cell mortality. Cell 85:27–37PubMedCrossRefGoogle Scholar
  92. Shigeta T, Umeda M, Komatsubara H, Komori T (2008) Lymph node and pulmonary metastases after transplantation of oral squamous cell carcinoma cell line (HSC-3) into the subcutaneous tissue of nude mouse: Detection of metastases by genetic methods using beta-globin and mutant p53 genes. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 105:486–490Google Scholar
  93. Shintani S, Mihara M, Nakahara Y, Aida T, Tachikawa T, Hamakawa H (2002) Lymph node metastasis of oral cancer visualized in live tissue by green fluorescent protein expression. Oral Oncol 38:664–669PubMedCrossRefGoogle Scholar
  94. Shintani S, Li C, Mihara M, Nakashiro K, Hamakawa H (2003) Gefitinib (“Iressa”), an epidermal growth factor receptor tyrosine kinase inhibitor, mediates the inhibition of lymph node metastasis in oral cancer cells. Cancer Lett 201:149–155PubMedCrossRefGoogle Scholar
  95. Shklar G (1966) Cortisone and hamster buccal pouch carcinogenesis. Cancer Res 26:2461–2463PubMedGoogle Scholar
  96. Silva RN, Ribeiro DA, Salvadori DM, Marques ME (2007) Placental glutathione S-transferase correlates with cellular proliferation during rat tongue carcinogenesis induced by 4-nitroquinoline 1-oxide. Exp Toxicol Pathol 59:61–68PubMedCrossRefGoogle Scholar
  97. Simon C, Nemechek AJ, Boyd D, O’Malley BW Jr, Goepfert H, Flaitz CM, Hicks MJ (1998) An orthotopic floor-of-mouth cancer model allows quantification of tumor invasion. Laryngoscope 108:1686–1691PubMedCrossRefGoogle Scholar
  98. Stewart TA, Pattengale PK, Leder P (1984) Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 38:627–637PubMedCrossRefGoogle Scholar
  99. Strati K, Pitot HC, Lambert PF (2006) Identification of biomarkers that distinguish human papillomavirus (HPV)-positive versus HPV-negative head and neck cancers in a mouse model. Proc Natl Acad Sci USA 103:14152–14157PubMedCrossRefGoogle Scholar
  100. Swan EA, Jasser SA, Holsinger FC, Doan D, Bucana C, Myers JN (2003) Acquisition of anoikis resistance is a critical step in the progression of oral tongue cancer. Oral Oncol 39:648–655PubMedCrossRefGoogle Scholar
  101. Take Y, Umeda M, Teranobu O, Shimada K (1999) Lymph node metastases in hamster tongue cancer induced with 9, 10-dimethyl-1, 2-benzanthracene: association between histological findings and the incidence of neck metastases, and the clinical implications for patients with tongue cancer. Br J Oral Maxillofac Surg 37:29–36PubMedCrossRefGoogle Scholar
  102. Tan MH, Holyoke ED, Goldrosen MH (1977) Murine colon adenocarcinoma: Syngeneic orthotopic transplantation and subsequent hepatic metastases. J Natl Cancer Inst 59:1537–1544PubMedGoogle Scholar
  103. Tang XH, Knudsen B, Bemis D, Tickoo S, Gudas LJ (2004) Oral cavity and esophageal carcinogenesis modeled in carcinogen-treated mice. Clin Cancer Res 10:301–313PubMedCrossRefGoogle Scholar
  104. Varney ML, Olsen KJ, Mosley RL, Bucana CD, Talmadge JE, Singh RK (2002) Monocyte/macrophage recruitment, activation and differentiation modulate interleukin-8 production: A paracrine role of tumor-associated macrophages in tumor angiogenesis. In Vivo 16:471–477PubMedGoogle Scholar
  105. Vered M, Allon I, Buchner A, Dayan D (2007) Stromal myofibroblasts and malignant transformation in a 4NQO rat tongue carcinogenesis model. Oral Oncol 43:999–1006PubMedCrossRefGoogle Scholar
  106. Wallenius K, Lekholm U (1973) Oral cancer in rats induced by the water-soluble carcinogen 4-nitrochinoline N-oxide. Odontol Revy 24:39–48PubMedGoogle Scholar
  107. Weiss L (1996) Metastatic inefficiency: Intravascular and intraperitoneal implantation of cancer cells. Cancer Treat Res 82:1–11PubMedGoogle Scholar
  108. Williams ME, Gaffey MJ, Weiss LM, Wilczynski SP, Schuuring E, Levine PA (1993) Chromosome 11Q13 amplification in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 119:1238–1243PubMedGoogle Scholar
  109. Wong DT (1987) Amplification of the c-erb B1 oncogene in chemically-induced oral carcinomas. Carcinogenesis 8:1963–1965PubMedCrossRefGoogle Scholar
  110. Xie X, Brunner N, Jensen G, Albrectsen J, Gotthardsen B, Rygaard J (1992) Comparative studies between nude and scid mice on the growth and metastatic behavior of xenografted human tumors. Clin Exp Metastasis 10:201–210PubMedCrossRefGoogle Scholar
  111. Yamada T, Mogi M, Kage T, Ueda A, Nakajima J, Chino T (1992) Enhancement by cyclosporin A of metastasis from hamster cheek pouch carcinoma. Arch Oral Biol 37:593–596PubMedCrossRefGoogle Scholar
  112. Yamagiwa K, Ichikawa K (1977) Experimental study of the pathogenesis of carcinoma. CA Cancer J Clin 27:174–181PubMedCrossRefGoogle Scholar
  113. Yang M, Baranov E, Li XM, Wang JW, Jiang P, Li L, Moossa AR, Penman S, Hoffman RM (2001) Whole-body and intravital optical imaging of angiogenesis in orthotopically implanted tumors. Proc Natl Acad Sci USA 98:2616–2621PubMedCrossRefGoogle Scholar
  114. Yazici YD, Kim S, Jasser SA, Wang Z, Carter KB Jr, Bucana CD, Myers JN (2005) Antivascular therapy of oral tongue squamous cell carcinoma with PTK787. Laryngoscope 115:2249–2255PubMedCrossRefGoogle Scholar
  115. Yuan B, Heniford BW, Ackermann DM, Hawkins BL, Hendler FJ (1994) Harvey ras (H-ras) point mutations are induced by 4-nitroquinoline-1-oxide in murine oral squamous epithelia, while squamous cell carcinomas and loss of heterozygosity occur without additional exposure. Cancer Res 54:5310–5317PubMedGoogle Scholar
  116. Yuan B, Oechsli MN, Hendler FJ (1997) A region within murine chromosome 7F4, syntenic to the human 11q13 amplicon, is frequently amplified in 4NQO-induced oral cavity tumors. Oncogene 15:1161–1170PubMedCrossRefGoogle Scholar
  117. Zhang L, Hellstrom KE, Chen L (1994) Luciferase activity as a marker of tumor burden and as an indicator of tumor response to antineoplastic therapy in vivo. Clin Exp Metastasis 12:87–92PubMedCrossRefGoogle Scholar
  118. Zhang Z, Wang Y, Yao R, Li J, Lubet RA, You M (2006) p53 Transgenic mice are highly susceptible to 4-nitroquinoline-1-oxide-induced oral cancer. Mol Cancer Res 4:401–410PubMedCrossRefGoogle Scholar
  119. Zucker S, Cao J, Chen WT (2000) Critical appraisal of the use of matrix metalloproteinase inhibitors in cancer treatment. Oncogene 19:6642–6650PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Head and Neck Surgery-Unit 441University of Texas M D Anderson CancerHoustonUSA

Personalised recommendations