Rat brain tumor models in experimental neuro-oncology: The 9L, C6, T9, F98, RG2 (D74), RT-2 and CNS-1 gliomas

Journal of Neuro-Oncology

Volumn 36, Issue 1, 1998, Pages 91-102

  Barth, Rolf F ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Rat brain tumors: 9L, C6, T9, F98, RG2 (D74), RT 2, CNS 1

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AVIAN SARCOMA VIRUS; BIOCHEMISTRY; BRAIN CANCER; CANCER CELL CULTURE; CANCER RESEARCH; CANCER SURVIVAL; CELL GROWTH; GLIA CELL; GLIOMA; GLIOSARCOMA; IMMUNE RESPONSE; NONHUMAN; RAT; REPRODUCIBILITY; REVIEW;

ANIMALS; AVIAN SARCOMA VIRUSES; BRAIN NEOPLASMS; DISEASE MODELS, ANIMAL; GLIOMA; GLIOSARCOMA; RATS; RETROVIRIDAE INFECTIONS;

EID: 0031776473     PISSN: 0167594X     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1005805203044     Document Type: Review

References (152)

1. Gill TJ, Smith GJ, Wissler RW and Kunz HW: The rat as an experimental animal. Science 245: 269-276, 1989
2. Peckham JC: Experimental oncology. In: Baker HJ, Lindsey JR, Weisbroth SH (ed) The Laboratory Rat. Vol. II. Research Applications. Academic Press, New York 1980, pp 119-147
3. Janisch W: Tumors of the central nervous system. In: Turusov VS, Mohn U (ed) Pathology of Tumours in Laboratory Animals Volume I - Tumors of the Rat. International Agency for Research on Cancer, Lyon, France 1990, pp 67-689
4. Peterson DL, Sheridan PJ and Brown WE: Animal models for brain tumors: historical perspectives and future directions. J Neurosurg 80: 865-876, 1994
5. Maggio WW: Rodent glioma models. In: Perez-Polo JR (ed) Methods in Neurosciences, Vol. 30. Paradigms of Neural Injury. Academic Press Inc, San Diego 1996, pp 81-96
6. Ausman JI, Shapiro WR and Rail DP: Studies on the chemotherapy of experimental brain tumors: Development of an experimental model. Cancer Res 30: 2394-2400, 1970
7. Schold SC and Bigner DD: A review of animal brain tumor models that have been used for therapeutic studies. In: Walker MD (ed) Oncology of the Nervous System. Martinus Nijhoff Publishers, Boston 1983, pp 31-63
8. Bigner DD, Kvedar JP, Shaffer TC, Vick NA, Engel WK and Day ED : Factors influencing the cell type of brain tumors induced in dogs by Schmidt-Ruppin Rous sarcoma virus. J Neuropath Exp Neurol 31: 583-595, 1972
9. Bigner DD, Odom GL and Day ED: Brain tumors induced in dogs by the Schmidt-Ruppin strain of Rous sarcoma virus: neuropathological and immunological observations. J Neuropath Exp Neurol 28: 648-680, 1969
10. Ernestus RI, Wilmess LJ and Hoehn-Berlage M: Identification of intracranial liqor metastasis of experimental stereotactically implanted brain tumors by the tumor-selective MRI contrast agent MNTPPS. Clin Exp Metastas 10: 345-350, 1992
11. Druckrey H, Ivankovic S and Preussmann R. Selektive erzeugung maligner tumoren im gehirn und ruckenmark von ratten durch N-methyl-N-nitrosoharnstoff. Z Krebsforsch 25: 389-408, 1964
12. Benda P, Someda K, Messer J and Sweet WH : Morphological and immunochemical studies of rat glial tumors and clonal strains propagated in culture. J Neurosurg 34: 310-323, 1971
13. Schmidek HH, Nielsen SL, Schiller AL and Messer J: Morphological studies of rat brain tumors induced by N-nitrosomethylurea. J Neurosurg 34: 335-340, 1971
14. Swenberg JA, Koestner A and Wechsler W: The induction of tumors of the nervous system with intravenous methyl-nitrosourea. Lab Invest 26: 74-85, 1972
15. Swenberg JA, Koestner A, Wechsler W and Denlinger RH : Quantitative aspects of transplacental tumor induction with ethylnitrosourea in rats. Cancer Res 32: 2656-2660, 1972
16. Koestner A and Marushige K. Neurocarcinogenesis. In: Waalkes MP and Ward JM (eds) Carcinogenesis. Raven Press, Ltd., New York 1994, pp 301-337
17. He X, Archer GE, Wikstrand CJ, Morrison SL, Zalutsky MR, Bigner DD and Barta SK: Generation and characterization of a mouse/human chimeric antibody directed against extracellular matrix protein tenascin. J Neuroimmunol 52: 127-137, 1994
18. Mahaley MS, Gentry RE and Bigner D D : Immunobiology of primary intracranial tumors. J Neurosurg 47: 35-43, 1977
19. Mennel HD and Groneck P: Quantitative aspects of transplantation of experimentally induced tumors of the nervous system. Acta Neuropath 40: 145-150, 1977
20. Rama B, Spoerri O, Holzgraefe M and Mennel HD: Current brain tumour models with particular consideration of the transplantation techniques. Acta Neurochir 79: 35-41, 1986
21. Wilson CB: Brain tumor models for experimental therapy. In: Laerum OD, Bigner DD and Rajwesky MF (eds) Biology of Brain Tumors. International Union Against Cancer, Geneva 185-199, 1978
22. Barker M, Hoshino T, Gurcay O, Wilson CB, Nielsen SL, Downie R and Eliason J: Development of an animal brain tumor model and its response therapy with 1,3-bis (2-chloroethyl)-1-nitrosourea. Cancer Res 33: 976-986, 1973
23. Barker M, Deen DF and Baker DG: BCNU and X-ray therapy of intracerebral 9L rat tumors. Int J Radiation Oncology Biol Phys 5: 1581-1583, 1979
24. Kobayashi N, Allen N, Clendenon NR and Ko L: An improved rat brain-tumor model. J Neurosurg 53: 808-815, 1980
25. Clendenon NR, Barth RF, Gordon WA, Goodman JH, Alam F, Staubus AE, Boesel CP, Yates AJ, Moeschberger ML, Fairchild RG and Kalef-Ezra JA: Boron neutron capture therapy of a rat glioma. Neurosurgery 26: 47-55, 1990
26. Weizsacker M, Deen DF, Rosenblum ML, Hoshino T, Gutin PH and Barker M: The 9L rat brain tumor: description and application of an animal model. J Neurol 224: 183-192, 1981
27. Yoshida T, Shimizu K, Ushio Y, Hayakawa T, Mogami H and Sakamoto Y: The mechanism and overcoming of resistance in ACNU resistant sublines of C6 and 9L rat glioma. J Neurooncol 5: 195-203, 1987
28. Asai A, Shibui S, Barker M, Vanderlaan M, Gray JW and Hoshino T: Cell kinetics of rat 9L brain tumors determined by double labeling with iodo- and bromodeoxyuridine. J Neurosurg 73: 254-258, 1990
29. Fross RD, Warnke PC and Groothius DR: Blood flow and blood-to-tissue transport in 9L gliosarcomas: the role of the brain tumor model in drug delivery research. J Neurooncol 11: 185-197, 1991
30. Groothius DR, Fischer JM, Lapin G, Bigner DD and Vick NA: Permeability of different experimental brain tumor models to horseradish peroxidase. J Neuropathol Exp Neurol 41: 164-185, 1982
31. Groothius DR, Pasternak J, Fischer J, Blasberg RG, Bigner DD and Vick NA: Regional measurements of blood flow in experimental RG2 rat gliomas. Cancer Res 43: 3362-3367, 1983
32. Levin VA, Freeman-Dove M and Landahl HD : Permeability characteristics of brain adjacent to tumors in rats. Arch Neurol 32: 785-791, 1975
33. Warnke PC, Blasberg RG and Groothius DR: The effect of hyperosmotic blood-brain barrier disruption on blood-to-tissue transport in ENU-induced gliomas. Ann Neurol 22: 300-305, 1987
34. Rajan SS, Rosa L, Francisco J, Muraki A, Carvlin M and Tuturea E: MRI characterization of 9L-glioma in rat brain at 4.7 tesla. Magn Reson Imagin 8: 185-190, 1990
35. Wilkins DE, Raaphorst GP, Saunders JK, Sutherland GR and Smith ICP: Correlation between Gd-enhanced MR imaging and histopathology in treated and untreated 9L rat brain tumors. Magn Reson Imagin 13: 89-96, 1995
36. Wong KH, Wallen CA and Wheeler KT: Chemosensitization of the nitrosoureas by 2-nitroimidazoles in the subcutaneous 9L tumor model: pharmacokinetic and structureactivity considerations. Int J Radiation Oncology Biol Phys 18: 1043-1050, 1989
37. Blasberg RG, Groothius D and Molnar P: A review of hyperosmotic blood-brain barrier disruption in seven experimental brain tumor models. In: Johansson BB, Owman C and Widner H (eds) Pathophysiology of the Blood-Brain Barrier. Elsevier, Amsterdam 1990, pp 197-220
38. Groothius DR, Fischer JM Vick NA and Bigner D D : Comparative permeability of different glioma models to horseradish peroxidase. Cancer Treat Rep 65: 13-18, 1981
39. Wilson JT and Penar PL: The effect of A G M-1470 in an improved intracranial 9L gliosarcoma rat model. Neurol Res 16: 121-124, 1994
40. Barcellos-Hoff MH, Linfoot PA, Marton LJ and Deen DF: Production of stable phenotypes from 9L rat brain tumor multicellular spheroids treated with 1,3-bis (2-chloroethyl)-1-nitrosourea. Int J Cancer 52: 409-413, 1992
41. Wen P, Loeffler JS, Morris JH and Lampson LA: The effects of irradiation on major histocompatibility complex expression and lymphocytic infiltration in the normal rat brain and the 9L gliosarcoma brain tumor model. J Neuroimmunol 27: 239-244, 1990
42. Wen PY, Lampson MA and Lampson LA: Effects of γ-interferon on major histocompatibility complex antigen expression and lymphocytic infiltration in the 9L gliosarcoma brain tumor model: Implications for strategies of immunotherapy. J Neuroimmunol 36: 57-68, 1992
43. Vats TS, Morantz RA, Wood GW and Tilzer S: Study of effectiveness of bleomycin in rat brain tumor model intravenously and intracerebrally. Int J Radiation Ocology Biol Phys 5: 1527-1529, 1979
44. Kimler BF, Liu C, Evans RG and Morantz RA: Intracerebral chemotherapy in the 9L rat brain tumor model. J Neurooncol 14: 191-200, 1992
45. Kimler BF, Martin DF, Evans RG, Morantz RA and Vats TS: Combination of radiation therapy and intracranial bleomycin in the 9L rat brain tumor model. Int J Radiation Oncology Biol Phys 18: 1115-1121, 1990
46. Tamargo RJ, Leong KW and Brem H : Growth inhibition of the 9L glioma using polymers to release heparin and cortisone acetate. J Neurooncol 9: 131-138, 1990
47. Biola JJ, Agbaria RA, Walbridge S, Oshiro EM, Johns DG, Kelley JA, Oldfield EH and Ram Z: In situ cyclopentenyl cytosine infusion for the treatment of experimental brain tumors. Cancer Res 55: 1306-1309, 1995
48. Henderson SD, Kimler BR and Morantz RA: Radiation therapy of 9L rat brain tumors. Int J Radiation Oncology Biol Phys 7: 497-502, 1981
49. Fleshner M, Watkins LR, Redd JM, Kruse CA and Bellgrau D : A 9L gliosarcoma transplantation model for studying adoptive immunotherapy into the brains of conscious rats. Cell Transplant 1: 307-312, 1992
50. Kruse CA, Kong Q, Schiltz PM and Kleinschmidt-De-Masters BK: Migration of activated lymphocytes when adoptively transferred into cannulated rat brain. J Neuroimmunol 55: 11-21, 1994
51. Kruse CA, Lillehei KO, Mitchel DH, Kleinschmidt-De-Masters B and Bellgrau D: Analysis of interleukin 2 and various effector cell populations in adoptive immunotherapy of 9L rat gliosarcoma: allogeneic cytotoxic T lymphocytes prevent tumor take. Proc Natl Acad Sci USA 87: 9577-9581, 1990
52. Kruse CA, Schuiltz PM, Bellgrau D, Kong Q and Kleinschmidt-DeMasters BK: Intracranial administrations of single or multiple source allogeneic cytotoxic T lymphocytes: Chronic therapy for primary brain tumors. J Neurooncol 19: 161-168, 1994
53. Kruse CA, Mitchell DH, Kleinschmidt-DeMasters BK, Bellgrau D, Eule JM, Parra JR, Kong Q and Lillehei KO: Systemic chemotherapy combined with local adoptive immunotherapy cures rats bearing 9L gliosarcoma. J Neurooncol 15: 97-112, 1993
54. Kroll RA, Pagel MA, Muldoon LL, Roman- Goldstein S and Neu welt E A : Increasing volume of distribution to the brain with interstitial infusion: Dose, rather than convection, might be the most important factor. Neurosurgery 38: 746-754, 1996
55. Coderre JA, Joel DD, Micca PL, Nawrocky MM and Slatkin DN: Control of intracerebral gliosarcomas in rats by boron neutron capture therapy with p-boronophenylalanine. Radat Res 129: 290-296, 1992
56. Coderre JA, Makar MS, Micca PL, Nawrocky MM, Liu HB and Joel DD, Slatkin DN and Amols HI: Derivations of RBE's for the high-LET radiations of the 9L rat gliosarcoma in vitro and in vivo. Int J Radiation Oncology Biol Phys 27: 1121-1129, 1993
57. Coderre J, Rubin P, Freedman A, Hansen J, Wooding TS, Joel D and Gash D: Selective ablation of rat brain tumors by boron neutron capture therapy. Int J Radiation Oncology Biol Phys 28: 1067-1077, 1994
58. Barba D, Hardin J, Ray J and Gage FH: Thymidine kinase-mediated killing of rat brain tumors. J Neurosurg 79: 729-735, 1993
59. Boviatsis EJ, Chase M, Wei MX, Tamiya T, Hurford RK, Kowall NW, Tepper RI, Breakefield XO and Chiocca EA: Gene transfer into experimental brain tumors mediated by adenovirus, herpes simplex virus, and retrovirus vectors. Hum Gene Ther 5: 183-191, 1994
60. Boviatsis EJ, Park JS, Sena-Esteves M,Kramm CM, Chase M, Efird JT, Wei MX, Breakefield XO and Chiocca EA: Long-term survival of rats harboring brain neoplasms treated with ganciclovir and a herpes simplex virus vector that retains an intact thymidine kinase gene. Cancer Res 54: 5745-5751, 1994
61. Chiocca EA, Andersen JK, Takamiya Y, Martuza RL and Breakefield XO: Virus-mediated genetic treatment of rodent gliomas. In: Wolff JA (ed) Gene Therapeutics: Methods and Applications of Direct Gene Transfer. Birkhauser, Boston 1994, pp 245-262
62. Cool V, Pirotte B, Gerard C, Dargent JL, Baudson N, Levivier M, Goldman S, Hildebrand J, Brotchi J and Velu T: Curative potential of herpes simplex virus thymidine kinase gene transfer in rats with 9L gliosarcoma. Hum Gene Ther 7: 627-635, 1996
63. Jia WWG, McDermott M, Goldie J, Cynader M, Tan J and Tufaro F: Selective destruction of gliomas in immunocompetent rats by thymidine kinase-defective herpes simplex virus type 1. J Natl Cancer Inst 86: 1209-1215, 1994
64. Kim JH, Kim SH, Kolozsvary A, Brown SL, Kim OB and Freytag SO: Selective enhancement of radiation response of herpes simplex virus thymidine kinase transduced 9L gliosarcoma cells in vitro and in vivo by antiviral agents. Int J Radiation Oncology Biol Phys 33: 861-868, 1995
65. Kramm CM, Rainov NG, Seno-Esteves M, Chase M, Pechan PA, Chiocca EA and Breakefield XO. Herpes vector-mediated delivery of marker genes to disseminated central nervous system tumors. Hum Gene Ther 7: 291-300, 1996
66. Lampson LA, Lampson MA and Dunne AD. Exploiting the lacZ reporter gene for quantitative analysis of disseminated tumor growth within the brain: Use of the lacZ gene product as a tumor antigen, for evaluation of antigenic modulation, and to facilitate image analysis of tumor growth in situ. Cancer Res 53: 176-182, 1993
67. Nam M, Johnston P, Lal B, Indurti R, Wilson MA and Laterra J: Endothelial cell-based cytokine gene delivery inhibits 9L glioma growth in vivo. Brain Res 731: 161-170, 1996
68. Rainov NG, Zimmer C, Chase M, Kramm CM, Chiocca EA, Weissleder R and Breakefield XO : Selective uptake of viral and monocrystalline particles delivered intra-arterially to experimental brain neoplasms. Hum Gene Ther 6: 1543-1552, 1995
69. Ram Z, Walbridge S, Heiss JD, Culver KW, Blaese RM and Oldfield EH: In vivo transfer of the human interleukin-2 gene: negative tumoricidal results in experimental brain tumors. J Neurosurg 80: 535-540, 1994
70. Ram Z, Walbridge S, Shawker T, Culver KW, Blaese RM and Oldfield EH. The effect of thymidine kinase transduction and ganciclovir therapy on tumor vasculature and growth of 9L gliomas in rats. J Neurosurg 81: 256-260, 1994
71. Vincent AJPE, Vogels R, Someren GW, Esandi MC, Noteboom JL, Avezaat CJJ, Vecht C, Bekkum DWV, Valerio D, Bout A and Hoogerbrugge PM: Herpes simplex virus thymidine kinase gene therapy for rat malignant brain tumors. Hum Gene Ther 7: 197-205, 1996
72. Viola JJ, Ram Z,Walbridge S, Oshiro EM, Trapnell B,Tao-Cheng JH and Oldfield EH: Adenovirally mediated gene transfer into experimental solid brain tumors and leptomeningeal cancer cells. J Neurosurg 82: 70-76, 1995
73. Blume MR, Wilson CB and Vasquez DA: Immune response to a transplantable intracerebral glioma in rats. In: Sane K, Ishi S and LeVay D (eds) Recent Progress in Neurologic Surgery. Excerpta Medica, Amsterdam 129-134, 1974
74. Denlinger RH, Axler DA, Koestner A and Liss L: Tumor-specific transplantation immunity to intracerebral challenge with cells from a methylnitrosourea-induced brain tumor. J Med 6: 249-259, 1975
75. Morantz RA, Wood GW, Foster M, Clark M and Gollahon K: Macrophages in experimental and human brain tumors Part 1: Studies of the macrophage content of experimental rat brain tumors of varying immunogenicity. J Neurosurg 50: 298-403, 1979
76. Barba D, Hardin J, Sadelain M and Gage FH: Development of anti-tumor immunity following thymidine kinase-mediated killing of experimental brain tumors. Proc Natl Acad Sci USA 91: 4348-4352, 1994
77. Tapscott SJ, Miller AD, Olson JM, Berger MS, Groudine M and Spence AM: Gene therapy of rat 9L gliosarcoma tumors by transduction with selectable genes does not require drug selection. Proc Natl Acad Sci USA 91: 8185-8189, 1994
78. Chen CY, Chang YN, Ryan P, Linscott M, McGarrity GJ and Chiang YL: Effect of herpes simplex virus thymidine kinase expression levels on ganciclovir-mediated cytotoxicity and the 'bystander effect'. Hum Gene Ther 6: 1467-1476, 1995
79. Culver KW, Ram CZ, Wallbridge S, Ishii H, Oldfield EH and Blaese RM: In vivo gene tranfer with retroviral vector-producer cells for treatment of experimental brain tumors. Science 256: 1550-1552, 1992
80. Freeman SM, Abboud CN, Whartenby KA, Packman CH, Koeplin DS, Moolten FL and Abraham GN: The 'bystander effect': Tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res 53: 5274-5283, 1993
81. Moolten FL: Tumor chemosensitivity conferred by inserted herpes thymidine kinase genes: Paradigm for a prospective cancer control strategy. Cancer Res 46: 5276-5281, 1986
82. Kida Y, Cravioto H, Hochwald GM, Hochgeschwender U and Ransohoff J: Immunity to transplantable nitrosourea-induced neurogenic tumors II. Immunoprophylaxis of tumors of the brain. J Neuropathol Exp Neurol 42: 122-135, 1983
83. Shibuya N, Hochgeschwender U, Kida Y, Hochwald GM, Thorbecke GJ and Cravioto H: Immunity to transplantable nitrosourea-induced neurogenic tumors. III. Systemic adoptive transfer of immunity. J Neuropathol Exp Neurol 43: 426-438, 1984
84. Harada K, Yoshida J, Mizuno M, Kurisu K and Uozumi T: Growth inhibition of intracerebral rat glioma by transfection-induced human interferon-β. J Surg Oncol 59: 105-109, 1995
85. Graf M, Masunaka I, Van Eden M, Granger G and Jacques D : T9 rat glioma cells secreting human TNF-α immunize Fischer rats against untransfected T9 and 9L gliomas. Proc Amer Assoc Cancer Res 35: A2978, 1994
86. Benda P, Lightbody J, Sato G, Levine L and Sweet W: Differentiated rat glial cell strain in tissue culture. Science 26: 370-371, 1968
87. Pfeiffer SE, Herschman HR, Lightbody J and Sato G: Synthesis by a clonal line of rat glial cells of a protein to the nervous system. J Cell Physiol 75: 329-340, 1969
88. Yoshida T, Shimizu K, Ushio Y, Hayakawa T, Mogami H and Sakamoto Y: Enhanced effect of reserpine upon growth-inhibitory action of ACNU on ACNU-resistant C6 glioma. Br J Cancer 53: 773-777, 1986
89. Kondziolka D, Somaza S, Comey C, Lunsford LD, Claassen D, Pandalai S, Maitz A, Flickinger JR: Radiosurgery and fractionated radiation therapy: Comparison of different techniques in an in vivo rat glioma model. J. Neurosurg 84: 1033-1038, 1996
90. Carson WE, Jakowatz JG, Yamamoto R, Fitzgerald T, Gupta S, Vayuvegula B, Lucci JA, Beckman MT, Dulkanchainun S, Granger GA and Jeffes EW: Rat mitogen-stimulated lymphokine-activated T killer cells: Production and effect on C6 glioma cells in vitro and in vivo in the brain of Wistar rats. J Immunother 10: 131-140, 1991
91. Kaye AH, Morstyn G and Ashcroft RG: Uptake and retention of hematoporphyrin derivative in an in vivo/in vitro model of cerebral glioma. Neurosurgery 17: 883-890, 1985
92. Kaye AH,Morstyn G, Garder I and Pyke K: Development of a xenograft glioma model in mouse brain. Cancer Res 46: 1367-1373, 1986
93. Chen SH, Shine HD, Goodman JC, Grossman RG and Woo SLC: Gene therapy for brain tumors: regression of experimental gliomas by adenovirus-mediated gene transfer in vivo. Proc Natl Acad Sci USA 91: 3054-3057, 1994
94. Maron A, Gustin T, LeRoux A, Mottet I, Dedieu JF, Brion JP, Demeure R, Perricaudet M and Octave JN: Gene therapy of rat C6 glioma using adenovirus-mediated transfer of the herpes simplex virus thymidine kinase gene: Long-term follow-up by magnetic resonance imaging. Gene Therapy 3: 315-322, 1996
95. Maron A, Gustin T, Mottet I, Demeure R and Octave JN: Ganciclovir mediated regression of rat brain tumors expressing the herpes simplex virus thymidine kinase imaged by magnetic resonance. J Neurooncol 24: 259-265, 1995
96. Trojan J, Johnson TR, Rudin SD, Ilan J, Tykocinski ML and Ilan J: Treatment and prevention of rat glioblastoma by immunogenic C6 cells expressing antisense insulin-like growth factor I RNA. Science 259: 94-97, 1993
97. Johnson TR, Trojan J, Rudin SD, Ilan J, Tykocinski ML and Ilan J. Evoking an immune response to glioblastoma cells transfected with episome-based plasmid expressing antisense transcripts to insulin-like growth factor I. In: Levine AJ and Schmidek HH (eds) Molecular Genetics of Nervous System Tumors. Wiley-Liss, Inc., New York 387-400, 1993
98. Nagano N, Sasaki H, Aoyagi M and Hirakawa K: Invasion of experimental rat brain tumor: Early morphological changes following microinjection of C6 glioma cells. Acta Neuropathol 86: 117-125, 1993
99. San-Galli F, Vrignaud P, Robert J, Coindre JM and Cohadon F: Assessment of the experimental model of transplanted C6 glioblastoma in Wistar rats. J Neurooncol 7: 299-304, 1989
100. Bernstein JJ, Laws ER, Levine KV, Wood LR, Tadvalkar G and Goldberg WJ: C6 glioma-astrocytoma cell and fetal astrocyte migration into artificial basement membrane: a permissive substrate for neural tumors but not fetal astrocytes. Neurosurgery 28: 652-658, 1991
101. Chicoine MR and Silbergeld DL: Invading C6 glioma cells maintaining tumorigenicity. J Neurosurg 83: 665-671, 1995
102. Farrel ICL and Shivers RR: Capillary junctions of the rat are not affected by osmotic opening of the blood-brain barrier. Acta Neuropathol 63: 179-189, 1984
103. Hurter T and Mennel HD : Experimental brain tumors and edema in rats. Acta Neuropathol 55: 105-111, 1981
104. Ohnishi T, Sher PB, Posner JB and Shapiro WR: Increased capillary permeability in rat brain induced by factors secreted by cultured C6 glioma cells: role in peritumoral brain edema. J Neurooncol 10: 13-25, 1991
105. Rapoport SI and Robinson PJ: A therapeutic role for osmotic opening of the blood-brain barrier. Re-evaluation of literature and importance of source-sink relations between brain and tumor. In: Johansson BB, Owman C and Widner H (eds), Pathophysiology of the Blood-Brain Barrier. Elsevier, Amsterdam 1990, pp 167-181
106. Rapoport SI: Osmotic opening of the blood-brain barrier. Ann Neurol 24: 677-684, 1988
107. Steinbok P, Mahaley MS U R, Varia MA, Lipper S, Mahaley J, Dalzell JG and Bigner DD: Treatment of autochthonous rat brain tumors with fractionated radiotherapy the effects of graded radiation doses and of combined therapy with BNCU or steroids. J Neurosurg 53: 68-72, 1980
108. Abramovitch R, Meir G and Neeman M: Neovascularization induced growth of implanted C6 glioma multicellular spheroids: Magnetic resonance microimaging. Cancer Res 55: 1956-1962, 1995
109. Farrell CL, Stewart PA and Del Maestro RF: A new glioma model in rat: The C6 spheroid impantation technique permeability and vascular characterization. J Neurooncol 4: 403-415, 1987
110. Bradshaw SL, Naus CCG, Zhu D, Kidder GM, D'Ercole AJ and Han VKM: Alterations in the synthesis of insulin-like growth factor binding proteins and insulin-like growth factors in rat C6 glioma cells transfected with a gap junction connexin 43 cDNA. Regul Pept 48: 99-112, 1993
111. Bradshaw SL, Naus CCG, Zhu D, Kidder GM and Han VKM: Insulin-like growth factor binding protein-4 gene expression is induced by transfection of gap junction connexin43 gene in a C6 glioma cell line. Growth Regul 3: 26-29, 1993
112. Fontana A, McAdam KPWJ, Kristensen F and Weber E: Biological and biochemical characterization of an interleukin 1-like factor from rat C6 glioma cells. Eur J Immunol 13: 685-689, 1983
113. Resnicoff M, Li W, Basak S, Herlyn D, Baserga R and Rubin R: Inhibition of rat C6 glioblastoma tumor growth by expression of insulin-like growth factor I receptor antisense mRNA. Cancer Immunol Immunother 42: 64-68, 1996
114. Resnicoff M, Sell C, Rubini M, Coppola D, Ambrose D, Baserga R and Rubin R: Rat glioblastoma cells expressing an antisense RNA to the insulin-like growth factor-1 (IGF-1) receptor are nontumorigenic and induce regression of wild-type tumors. Cancer Res 54: 2218-2222, 1994
115. Mokry J, Nemecek S, Adler J and Dedic K: Inoculation of C6 cell suspension into the brain of adult rats: immunohistochemical study. Funct Dev Morphol 3: 175-180, 1993
116. M1 into rat glioma C6 cells renders them susceptible to growth inhibition by the B subunit of cholera toxin. Biochim Biophys Acta 969: 249-256, 1988
117. Ko L, Koestner A and Wechsler W: Morphological characterization of nitrosourea-induced glioma cell lines and clones. Acta Neuropathol 51: 23-31, 1980
118. Vinores SA and Koestner A: The effect of nerve growth factor on undifferentiated glioma cells. Cancer Lett 10: 309-318, 1980
119. Kaneko S, Allen NJ, Clendenon NR and Kartha M: Treatment schedule of combination using radiation and ACNU in the experimental brain tumors. Neurol Med Chir 23: 849-855, 1983
120. Tzeng J-J, Barth RF, Clendenon NR and Gordon WA: Adoptive immunotherapy of a rat glioma using lymphokine-activated killer cells and interleukin-2. Cancer Res 50: 4338-4343, 1990
121. Barth RF, Yang W, Rotaru JH, Moeschberger ML, Joel DD, Nawrocky MM, Goodman JH and Soloway AH: Boron neutron capture therapy of brain tumors: Enhanced survival following intracarotid injection of either sodium borocaptate or borophenylalanine with or without blood brain barrier disruption. Cancer Res 57: 1129-1136, 1997
122. Matalka KZ, Barth RF, Staubus AE, Moeschberger ML and Coderre JA: Neutron capture therapy of a rat glioma using boronophenylalanine as a capture agent. Radiat Res 137: 44-51, 1994
123. Tzeng J-J, Earth RF, Orosz CG and James SM: Phenotype and functional activity of tumor-infiltrating lymphocytes isolated from immunogenic and nonimmunogenic rat brain tumors. Cancer Res 51: 2373-2378, 1991
124. Barba D, Bloomer U, Silva M and Gage FH : Tumor immunity, immunizations and herpes simplex virus-thymidine kinase mediated tumor regression. Abstracts First Scientific Meeting Soc Neuro-Oncol Nov 8-10, 1996 Santa Fe, New Mexico
125. Gyngell ML, Hoehn-Berlage M, Kloiber O, Michaelis T, Ernestus RI, Horstermann D and Frahm J: Localized proton NMR spectroscopy of experimental gliomas in rat brain in vivo. NMR Biomed 5: 335-340, 1992
126. Bockhorst K, Els T, Kohno K and Hoehn-Berlage M: Localization of experimental brain tumors in MRI by gadolinum porphyrin. Acta Neurochir 60: 347-349, 1994
127. Els T, Bockhorst K and Hoehn-Berlage M: NMR contrast enhancement of brain tumors. Comparison of the blood brain barrier tracer GdDTPA and the tumor-selective contrast agent in MnTPPS. MAGMA 1: 126-133, 1993
128. Hossmann KA, Mies G, Paschen W, Szabo E and Wechsler W: Regional metabolism of experimental brain tumors. Acta Neuropathol 69: 139-147, 1986
129. Eis M, Els T and Hoehn-Berlage: High resolution quantitative relaxation and diffusion MRI of three different experimental brain tumors in rat. MRM 34: 835-844, 1995
130. Eis M, Els T, Hoehn-Berlage M and Hossmann KA Quantitative diffusion MR imaging of cerebral tumor and edema. Acta Neurochir 60: 344-346, 1994
131. Judy KD, Olivi A, Buahin KG, Bomb A, Epstein JI, Colvin OM and Brem H: Effectiveness of controlled release of a cyclophosphamide derivative with polymers against rat gliomas. J Neurosurg 82: 481-486, 1995
132. Yang W, Barth RF, Rotaru JH, Joel DD, Nawrocky MM, Moeschberger ML, Goodman JH and Soloway AH: Boron neutron capture therapy of brain tumors: enhanced survival following intracarotid injection of sodium borocaptate with or without blood-brain barrier disruption. Int J Radiation Oncology Biol Phys 37: 663-672, 1997
133. Yang W, Barth RF, Rotaru JH, Joel DD, Nawrocky BA and Goodman J: Enhanced survival of glioma bearing rats following boron neutron capture therapy with osmotic blood-brain barrier disruption and intracarotid injection of boronophenylalanine. J Neurooncol 33: 59-70, 1997
134. Boucher Y, Saiehl H, Witwer B, Harsh GR and Jain RK: Interstitial fluid pressure in intracranial tumours in patients and in rodents. Br J Cancer 75: 529-536, 1997
135. Ernestus RI, Rohn F, Hossmann KA and Paschen W: Polyamine metabolism in experimental brain tumors of rat. J Neurochem 60:417-422, 1993
136. Aas AT, Brun A, Blennow C, Stromblad S and Salford LG: The RG2rat glioma model. J Neurooncol 23: 175-183, 1995
137. Groothius DR, Fischer JM, Pasternak JF, Blasberg RG and Bigner DD: Regional measurements of blood-to-tissue transport in transplanted RG2 rat gliomas. Cancer Res 43: 3368-3373, 1983
138. Ceberg CP, Brun A, Kahl SB, Koo MS, Persson BRR and Salford LG: A comparative study on the pharmacokinetics and biodistribution of boronated porphyrin (BOPP) and sulfhydryl boron hydride (BSH) in the RG2 rat glioma model. J Neurosurg 83: 86-92, 1995
139. Ceberg CP, Brun A, Mir LM, Persson BRR and Salford LG: Enhanced boron uptake in RG2 rat gliomas by electropermeabilization in vivo-a. new possibility in boron neutron capture therapy. Anti-Cancer Drug 5: 463-466, 1994
140. Molnar P, Lapin GD and Groothius DR: The effects of dexamethasone on experimental brain tumors: I. Transcapillary transport and blood flow in RG-2 gliomas. J Neurooncol 25: 19-28, 1995
141. Devineni D, Klein-Szanto A and Gallo JM: Tissue distribution of methotrexate following administration as a solution and as a magnetic microsphere conjugate in rats bearing brain tumors. J Neurooncol 24: 143-152, 1995
142. Devineni D, Klein-Szanto A and Gallo JM: In vivo microdialysis to characterize drug transport in brain tumors: analysis of methotrexate uptake in rat glioma-2 (RG-2)-bearing rats. Cancer Chemother Pharmacol 38: 499-507, 1996
143. Gallo JM, Varkonyi P, Hassan EE and Groothius DR: Targeting anticancer drugs to the brain: II. Physiological pharmacokinetic model of oxantrazole following intraarterial administration to rat glioma-2 (RG-2) bearing rats. J Pharmacokinet Biopharm 21: 575-592, 1993
144. Tjuvajev J, Gansbacher B, Desai R, Beattie B, Kaplitt M, Matei C, Koutcher J, Gilboa E and Blasberg R: RG-2 glioma growth attenuation and severe brain edema caused by local production of interleukin-2 and interferon-γ. Cancer Res 55: 1902-1910, 1995
145. Grove AS, DiChiro G and Rabotti GF: Experimental brain tumors, with a report of those induced in dogs by Rous sarcoma virus. J Neurosurg 26: 465-477, 1967
146. Copeland DD, Talley FA and Bigner DD: The fine structure of intracranial neoplasms induced by the inoculation of avian sarcoma virus in neonatal and adult rats. Am J Pathol 83: 149-176, 1976
147. Tabuchi K, Nushimoto A, Matsumoto K, Satoh T, Nakasone S, Fujiwara T and Ogura H : Establishment of a brain-tumor model in adult monkeys. J Neurosurg 63: 912-916, 1985
148. Steinbok P, Mahaley MS, U R, Zinn DC, Lipper S, Mahaley JL and Bigner DD : Synergism between B CNU and irradiation in the treatment of anaplastic gliomas in in vivo study using the avian sarcoma virus-induced glioma model. J Neurosurg 51: 581-586, 1979
149. Beckman WC, Powers SK, Brown JT, Gillespie GY, Bigner DD and Camps JL: Differential retention of rhodamine 123 by avian sarcoma virus-induced glioma and normal brain tissue of the rat in vivo. Cancer 59: 266-270, 1987
150. Watts RG and Merchant RE: Cerebrovascular effects and tumor kinetics after a single intratumoral injection of human recombinant interleukin-2 alone or in combination with intravenous chemotherapy in a rat model of glioma. Neurosurgery 31: 89-99, 1992
151. Rice CD and Merchant RE: Systemic treatment with murine recombinant interleukin-1β inhibits the growth and progression of malignant glioma in the rat. J Neurooncol 13: 43-55, 1992
152. Kruse CA, Molleston MC, Parks EP, Schiltz PM, Kleinschmidt-DeMasters BK and Hickey WF: A rat glioma model, CNS-1, with invasive characteristics similar to those of human gliomas: a comparison to 9L gliosarcoma. J Neurooncol 22: 191-200, 1994