Optimization of adenoviral vector-mediated transgene expression in the canine brain in vivo, and in canine glioma cells in vitro

Neuro-Oncology

Volumn 9, Issue 3, 2007, Pages 245-258

  Candolfi, Marianela ^a   Pluhar, G Elizabeth ^b   Kroeger, Kurt ^a   Puntel, Mariana ^a   Curtin, James ^a   Barcia, Carlos ^a   Muhammad, A K M Ghulam ^a   Xiong, Weidong ^a   Liu, Chunyan ^a   Mondkar, Sonali ^a   Kuoy, William ^a   Kang, Terry ^a   McNeil, Elizabeth A ^b   Freese, Andrew B ^b   Ohlfest, John R ^b   Moore, Peter ^c   Palmer, Donna ^d   Ng, Phillip ^d   Young, John D ^e   Lowenstein, Pedro R ^a   Castro, Maria G ^a,e   more..

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Brain inflammation; Canine; Flt3L; Gene therapy; Glioma; Gutless adenoviral vectors; HSV1 TK

Indexed keywords

ADENOVIRUS VECTOR; BETA GALACTOSIDASE; DOXYCYCLINE; FLT3 LIGAND; GANCICLOVIR; TETRACYCLINE; THYMIDINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; ASTROCYTE; CANCER MODEL; CANCER SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOMEGALOVIRUS; DOG; DRUG CYTOTOXICITY; ENZYME ACTIVITY; GENE EXPRESSION; GENE SEQUENCE; GLIOBLASTOMA; GLIOMA; GLIOMA CELL; HERPES SIMPLEX VIRUS 1; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MARKER GENE; NONHUMAN; PROMOTER REGION; TRANSGENE;

ADENOVIRIDAE; ANIMALS; BETA-GALACTOSIDASE; BRAIN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CYTOMEGALOVIRUS; DOGS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE THERAPY; GENETIC ENGINEERING; GENETIC VECTORS; GLIOMA; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICE; MICROSCOPY, CONFOCAL; PROMOTER REGIONS (GENETICS); PROTEIN-TYROSINE KINASES; TRANSDUCTION, GENETIC; TRANSGENES; VIRAL PROTEINS;

EID: 34547445754     PISSN: 15228517     EISSN: None     Source Type: Journal    
DOI: 10.1215/15228517-2007-012     Document Type: Article

References (59)

1. Castro MG, Cowen R, Williamson IK, et al. Current and future strategies for the treatment of malignant brain tumors. Pharmacol Ther. 2003;98:71-108.
2. Chiocca EA. Oncolytic viruses. Nat Rev Cancer. 2002;2:938-950.
3. Curtin JF, King GD, Candolfi M, et al. Combining cytotoxic and immune-mediated gene therapy to treat brain tumors. Curr Top Med Chem. 2005;5:1151-1170.
4. Gomez-Manzano C, Yung WK, Alemany R, Fueyo J. Genetically modified adenoviruses against gliomas: from bench to bedside. Neurology. 2004;63:418-426.
5. King GD, Curtin JF, Candolfi M, Kroeger K, Lowenstein PR, Castro MG. Gene therapy and targeted toxins for glioma. Curr Gene Ther. 2005;5:535-557.
6. Prados MD, Levin V. Biology and treatment of malignant glioma. Semin Oncol. 2000;27(Suppl 6):1-10.
7. Castro MG, Curtin J, King GD, et al. Novel gene therapeutic approaches to brain cancer. In: Castro MG, Lowenstein PR, eds. Gene Therapy for Neurological Disorders. New York: Taylor and Francis; 2006:229-264.
8. Chiocca EA, Abbed KM, Tatter S, et al. A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. Mol Ther. 2004;10:958-966.
9. Fueyo J, Alemany R, Gomez-Manzano C, et al. Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. J Natl Cancer Inst. 2003;95:652-660.
10. Germano IM, Fable J, Gultekin SH, Silvers A. Adenovirus/herpes simplex-thymidine kinase/ganciclovir complex: preliminary results of a phase I trial in patients with recurrent malignant gliomas. J Neurooncol. 2003;65:279-289.
11. Immonen A, Vapalahti M, Tyynela K, et al. AdvHSV-tk gene therapy with intravenous ganciclovir improves survival in human malignant glioma: a randomised, controlled study. Mol Ther. 2004;10:967-972.
12. Lang FF, Bruner JM, Fuller GN, et al. Phase I trial of adenovirus-mediated p53 gene therapy for recurrent glioma: biological and clinical results. J Clin Oncol. 2003;21:2508-2518.
13. Sandmair AM, Loimas S, Puranen P, et al. Thymidine kinase gene therapy for human malignant glioma, using replication-deficient retroviruses or adenoviruses. Hum Gene Ther. 2000;11:2197-2205.
14. Ali S, Curtin JF, Zirger JM, et al. Inflammatory and anti-glioma effects of an adenovirus expressing human soluble Fms-like tyrosine kinase 3 ligand (hsFlt3L): treatment with hsFlt3L inhibits intracranial glioma progression. Mol Ther. 2004;10:1071-1084.
15. Ali S, King GD, Curtin JF, et al. Combined immunostimulation and conditional cytotoxic gene therapy provide long-term survival in a large glioma model. Cancer Res. 2005;65:7194-7204.
16. Tyminski E, Leroy S, Terada K, et al. Brain tumor oncolysis with replication-conditional herpes simplex virus type 1 expressing the prodrug-activating genes, CYP2B1 and secreted human intestinal carboxylesterase, in combination with cyclophosphamide and irinotecan. Cancer Res. 2005;65:6850-6857.
17. Herrlinger U, Jacobs A, Quinones A, et al. Helper virus-free herpes simplex virus type 1 amplicon vectors for granulocyte-macrophage colony-stimulating factor-enhanced vaccination therapy for experimental glioma. Hum Gene Ther. 2000;11:1429-1438.
18. Breen M. Development of molecular cytogenetic resources for the dog and application to the study of the comparative pathology of canine myeloid neoplasms. Paper presented at the 56th Annual Meeting of the American College of Veterinary Pathologists (ACVP) and 40th Annual Meeting of the American Society for Veterinary Clinical Pathology (ASVCP), Middleton, WI; 2005.
19. Braund K. Neoplasia of the nervous system. In: KG B, ed. Clinical Neurology in Small Animals: Localization, Diagnosis and Treatment. Ithaca, NY: International Veterinary Information Service; 2003. Available at http://www.ivis.org.
20. Foster ES, Carrillo JM, Patnaik AK. Clinical signs of tumors affecting the rostral cerebrum in 43 dogs. J Vet Intern Med. 1988;2:71-74.
21. Heidner GL, Kornegay JN, Page RL, Dodge RK, Thrall DE. Analysis of survival in a retrospective study of 86 dogs with brain tumors. J Vet Intern Med. 1991;5:219-226.
22. LeCouteur RA. Current concepts in the diagnosis and treatment of brain tumours in dogs and cats. J Small Anim Pract. 1999;40:411-416.
23. Lipsitz D, Higgins RJ, Kortz GD, et al. Glioblastoma multiforme: clinical findings, magnetic resonance imaging, and pathology in five dogs. Vet Pathol. 2003;40:659-669.
24. Lindblad-Toh K, Wade CM, Mikkelsen TS, et al. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature. 2005;438:803-819.
25. Cerletti M, Negri T, Cozzi F, et al. Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer. Gene Ther. 2003;10:750-757
26. Childers MK, Okamura CS, Bogan DJ, Bogan JR, Sullivan MJ, Kornegay JN. Myofiber injury and regeneration in a canine homologue of Duchenne muscular dystrophy. Am J Phys Med Rehabil. 2001;80:175-181.
27. High K. Gene transfer for hemophilia: can therapeutic efficacy in large animals be safely translated to patients? J Thromb Haemost. 2005;3:1682-1691.
28. Ponder KP, Melniczek JR, Xu L, et al. Therapeutic neonatal hepatic gene therapy in mucopolysaccharidosis VII dogs. Proc Natl Acad Sci USA. 2002;99:13102-13107.
29. Wood PA, Sisk DB, Styer E, Baker HJ. Animal model: ceroidosis (ceroid-lipofuscinosis) in Australian cattle dogs. Am J Med Genet. 1987;26:891-898.
30. Gerdes CA, Castro MG, Lowenstein PR. Strong promoters are the key to highly efficient, noninflammatory and noncytotoxic adenoviral-mediated transgene delivery into the brain in vivo. Mol Ther. 2000;2:330-338.
31. Xiong W, Goverdhana S, Sciascia SA, et al. Regulatable gutless adenovirus vectors sustain inducible transgene expression in the brain in the presence of an immune response against adenoviruses. J Virol. 2006;80:27-37.
32. Candolfi M, Curtin JF, Xiong W, et al. Effective high capacity gutless adenoviral vectors mediate transgene expression in human glioma cells. Mol Ther. 2006;14:371-381.
33. Lowenstein PR, Thomas CE, Umana P, et al. High-capacity, helper-dependent, "gutless" adenoviral vectors for gene transfer into the brain. Methods Enzymol. 2002;346:292-311.
34. Lowenstein PR. Virology and immunology of gene therapy, or virology and immunology of high MOI infection with defective viruses. Gene Ther. 2003;10:933-934.
35. Thomas CE, Schiedner G, Kochanek S, Castro MG, Lowenstein PR. Peripheral infection with adenovirus causes unexpected long-term brain inflammation in animals injected intracranially with first-generation, but not with high-capacity, adenovirus vectors: toward realistic long-term neurological gene therapy for chronic diseases. Proc Natl Acad Sci USA. 2000;97:7482-7487.
36. Thomas CE, Schiedner G, Kochanek S, Castro MG, Lowenstein PR. Preexisting antiadenoviral immunity is not a barrier to efficient and stable transduction of the brain, mediated by novel high-capacity adenovirus vectors. Hum Gene Ther. 2001;12:839-846.
37. Chirmule N, Propert K, Magosin S, Qian Y, Qian R, Wilson J. Immune responses to adenovirus and adeno-associated virus in humans. Gene Ther. 1999;6:1574-1583.
38. Ehrhardt A, Kay MA. Gutted adenovirus: a rising star on the horizon? Gene Ther. 2005;12:1540-1541.
39. Southgate T, Kingston P, Castro MG. Gene transfer into neural cells in vivo using adenoviral vectors. In: Gerfen CR, McKay R, Rogawski MA, Sibley DR, Skolnick P, eds. Current Protocols in Neuroscience. Vol 4. New York: John Wiley and Sons; 2000:23.21-23.40.
40. Umana P, Gerdes CA, Stone D, et al. Efficient FLPe recombinase enables scalable production of helper-dependent adenoviral vectors with negligible helper-virus contamination. Nat Biotechnol. 2001;19:582-585.
41. Goverdhana S, Puntel M, Xiong W, et al. Regulatable gene expression systems for gene therapy applications: progress and future challenges. Mol Ther. 2005;12:189-211.
42. Dewey RA, Morrissey G, Cowsill CM, et al. Chronic brain inflammation and persistent herpes simplex virus 1 thymidine kinase expression in survivors of syngeneic glioma treated by adenovirus-mediated gene therapy: implications for clinical trials. Nat Med. 1999;5:1256-1263.
43. Thomas CE, Birkett D, Anozie I, Castro MG, Lowenstein PR. Acute direct adenoviral vector cytotoxicity and chronic, but not acute, inflammatory responses correlate with decreased vector-mediated transgene expression in the brain. Mol Ther. 2001;3:36-46.
44. Candolfi M, Kroeger KM, Pluhar GE, et al. Adenoviral-mediated gene transfer into the canine brain in vivo. Neurosurgery. 2007;60:167-177; discussion, 178.
45. Rainov NG, Koch S, Sena-Esteves M, Berens ME. Characterization of a canine glioma cell line as related to established experimental brain tumor models. J Neuropathol Exp Neurol. 2000;59:607-613.
46. Smith-Arica JR, Morelli AE, Larregina AT, Smith J, Lowenstein PR, Castro MG. Cell-type-specific and regulatable transgenesis in the adult brain: adenovirus-encoded combined transcriptional targeting and inducible transgene expression. Mol Ther. 2000;2:579-587
47. Curtin JF, King GD, Barcia C, et al. Fms-like tyrosine kinase 3 ligand recruits plasmacytoid dendritic cells to the brain. J Immunol. 2006;176:3566-3577.
48. Stein VM, Czub M, Schreiner N, et al. Microglial cell activation in demyelinating canine distemper lesions. J Neuroimmunol. 2004;153:122-131.
49. Zirger JM, Liu C, Barcia C, Castro MG, Lowenstein PR. Immune regulation of transgene expression in the brain: B cells regulate an early phase of elimination of transgene expression from adenoviral vectors. Viral Immunol. 2006;19:508-517
50. Lowenstein PR, Castro MG. Progress and challenges in viral vector-mediated gene transfer to the brain. Curr Opin Mol Ther. 2002;4:359-371.
51. Zirger JM, Barcia C, Liu C, et al. Rapid upregulation of interferon-regulated and chemokine mRNAs upon injection of 108 international units, but not lower doses, of adenoviral vectors into the brain. J Virol. 2006;80:5655-5659.
52. Palmer D, Ng P. Improved system for helper-dependent adenoviral vector production. Mol Ther. 2003;8:846-852.
53. Palmer DJ, Ng P. Physical and infectious titers of helper-dependent adenoviral vectors: a method of direct comparison to the adenovirus reference material. Mol Ther. 2004;10:792-798.
54. Maleniak TC, Darling JL, Lowenstein PR, Castro MG. Adenovirus-mediated expression of HSV1-TK or Fas ligand induces cell death in primary human glioma-derived cell cultures that are resistant to the chemotherapeutic agent CCNU. Cancer Gene Ther. 2001;8:589-598.
55. Raper SE, Chirmule N, Lee FS, et al. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol Genet Metab. 2003;80:148-158.
56. Yang Y, Nunes FA, Berencsi K, Furth EE, Gonczol E, Wilson JM. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci USA. 1994;91:4407-4411.
57. Barcia C, Thomas CE, Curtin JF, et al. In vivo mature immunological synapses forming SMACs mediate clearance of virally infected astrocytes from the brain. J Exp Med. 2006;203:2095-2107.
58. Windeatt S, Southgate TD, Dewey RA, et al. Adenovirus-mediated herpes simplex virus type-1 thymidine kinase gene therapy suppresses oestrogen-induced pituitary prolactinomas. J Clin Endocrinol Metab. 2000;85:1296-1305.
59. Lai JF, Cheng HY, Cheng TL, et al. Doxycycline- and tetracycline- regulated transcriptional silencer enhance the expression level and transactivating performance of rtTA. J Gene Med. 2004;6:1403-1413.