Chimeric adeno-associated virus and bacteriophage: A potential targeted gene therapy vector for malignant glioma

Therapeutic Delivery

Volumn 5, Issue 9, 2014, Pages 975-990

  Asavarut, Paladd ^a   O'Neill, Kevin ^a   Syed, Nelofer ^a   Hajitou, Amin ^a,b  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b HAMAD BIN KHALIFA UNIVERSITY   (Qatar)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 4;

ADENO ASSOCIATED VIRUS; ANGIOGENESIS; BACTERIOPHAGE; BLOOD BRAIN BARRIER; CLINICAL EFFECTIVENESS; CLINICAL TRIAL (TOPIC); GENE SILENCING; GENE TARGETING; GENE THERAPY; GLIOBLASTOMA; HERPES SIMPLEX VIRUS; HUMAN; IMMUNOMODULATORY GENE THERAPY; MAMMAL CELL; MOLECULAR THERAPY; NONHUMAN; PHAGE DISPLAY; REVIEW; SUICIDE GENE THERAPY; VIRAL GENE THERAPY; ANIMAL; BRAIN NEOPLASMS; CAPILLARY PERMEABILITY; DEPENDOPARVOVIRUS; GENE EXPRESSION REGULATION; GENE TRANSFER; GENE VECTOR; GENETICS; GLIOMA; METABOLISM; PATHOLOGY; PROCEDURES; RNAI THERAPEUTICS;

ANIMALS; BACTERIOPHAGES; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CAPILLARY PERMEABILITY; DEPENDOVIRUS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; GLIOMA; HUMANS; RNAI THERAPEUTICS;

EID: 84908615263     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.14.58     Document Type: Review

References (161)

1. Verma IM, Somia N. Gene therapy - promises, problems and prospects. Nature 389(6648), 239-242 (1997).
2. Waehler R, Russell SJ, Curiel DT. Engineering targeted viral vectors for gene therapy. Nat. Rev. Genet. 8(8), 573-587 (2007). An important review that gives a thorough account of how viral vectors for gene delivery are engineered for targeted therapy.
3. Tobias A, Ahmed A, Moon KS, Lesniak MS. The art of gene therapy for glioma: a review of the challenging road to the bedside. J. Neurol. Neurosurg. Psychiatr. 84(2), 213-222 (2013). An essential up-to-date review of current gene therapy trials and therapeutic approaches used for treating malignant glioma.
4. Ojala DS, Amara DP, Schaffer DV. Adeno-associated virus vectors and neurological gene therapy. Neuroscientist doi:10.1177/1073858414521870 (2014).
5. Bevan AKK, Brian K. CNS Gene Therapy Utilizing Intravenously Administered Viral Vectors. In: Drug Delivery to the Brain, Hammarlund-Udenaes MDL, Elizabeth C.M, Thorne, Robert G. (Eds). Springer New York, NY, USA 485-499 (2014).
6. Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the blood-brain barrier. Nat. Med. 19(12), 1584-1596 (2013).
7. Engelhardt B, Liebner S. Novel insights into the development and maintenance of the blood-brain barrier. Cell Tissue Res. 355(3), 687-699 (2014).
8. Gerstner ER, Fine RL. Increased permeability of the blood-brain barrier to chemotherapy in metastatic brain tumors: establishing a treatment paradigm. J. Clin. Oncol. 25(16), 2306-2312 (2007).
9. Chow KH, Gottschalk S. Cellular immunotherapy for high-grade glioma. Immunotherapy 3(3), 423-434 (2011).
10. Pardridge WM. Drug and gene targeting to the brain with molecular Trojan horses. Nat. Rev. Drug Discov. 1(2), 131-139 (2002).
11. Coloma MJ, Lee HJ, Kurihara A et al. Transport across the primate blood-brain barrier of a genetically engineered chimeric monoclonal antibody to the human insulin receptor. Pharm. Res. 17(3), 266-274 (2000).
12. Pardridge WM, Boado RJ, Kang YS. Vector-mediated delivery of a polyamide ("peptide") nucleic acid analogue through the blood-brain barrier in vivo. Proc. Natl Acad. Sci. U.S.A 92(12), 5592-5596 (1995).
13. Dufes C, Al Robaian M, Somani S. Transferrin and the transferrin receptor for the targeted delivery of therapeutic agents to the brain and cancer cells. Ther. Deliv. 4(5), 629-640 (2013).
14. Wang D, El-Amouri SS, Dai M et al. Engineering a lysosomal enzyme with a derivative of receptor-binding domain of apoE enables delivery across the blood-brain barrier. Proc. Natl Acad. Sci. U.S.A 110(8), 2999-3004 (2013).
15. Jiang X, Xin H, Ren Q et al. Nanoparticles of 2-deoxy-D-glucose functionalized poly(ethylene glycol)-co-poly(trimethylene carbonate) for dual-targeted drug delivery in glioma treatment. Biomaterials 35(1), 518-529 (2014).
16. Demeule M, Beaudet N, Regina A et al. Conjugation of a brain-penetrant peptide with neurotensin provides antinociceptive properties. J. Clin. Invest. (2014).
17. Schneider SW, Ludwig T, Tatenhorst L et al. Glioblastoma cells release factors that disrupt blood-brain barrier features. Acta Neuropathol. 107(3), 272-276 (2004).
18. Wolburg H, Noell S, Fallier-Becker P, Mack AF, Wolburg-Buchholz K. The disturbed blood-brain barrier in human glioblastoma. Mol. Aspects Med. 33(5-6), 579-589 (2012).
19. Agarwal S, Manchanda P, Vogelbaum MA, Ohlfest JR, Elmquist WF. Function of the blood-brain barrier and restriction of drug delivery to invasive glioma cells: findings in an orthotopic rat xenograft model of glioma. Drug Metab. Dispos. 41(1), 33-39 (2013).
20. Fine RL, Chen J, Balmaceda C et al. Randomized study of paclitaxel and tamoxifen deposition into human brain tumors: implications for the treatment of metastatic brain tumors. Clin. Cancer Res. 12(19), 5770-5776 (2006).
21. Rosso L, Brock CS, Gallo JM et al. A new model for prediction of drug distribution in tumor and normal tissues: pharmacokinetics of temozolomide in glioma patients. Cancer Res. 69(1), 120-127 (2009).
22. Schwartzbaum JA, Fisher JL, Aldape KD, Wrensch M. Epidemiology and molecular pathology of glioma. Nat. Clin. Prac. Neurol. 2(9), 494-503; quiz 491 p following 516 (2006).
23. Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro-oncology 7(2), 134-153 (2005).
24. Ruoslahti E. Vascular zip codes in angiogenesis and metastasis. Biochem. Soc. Trans. 32(Pt3), 397-402 (2004).
25. Moller HG, Rasmussen AP, Andersen HH, Johnsen KB, Henriksen M, Duroux M. A systematic review of microRNA in glioblastoma multiforme: micro-modulators in the mesenchymal mode of migration and invasion. Mol. Neurobiol. 47(1), 131-144 (2013).
26. Rao SS, Nelson MT, Xue R et al. Mimicking white matter tract topography using core-shell electrospun nanofibers to examine migration of malignant brain tumors. Biomaterials 34(21), 5181-5190 (2013).
27. Hjelmeland AB, Lathia JD, Sathornsumetee S, Rich JN. Twisted tango: brain tumor neurovascular interactions. Nat. Neurosci. 14(11), 1375-1381 (2011).
28. Rubenstein BM, Kaufman LJ. The role of extracellular matrix in glioma invasion: a cellular Potts model approach. Biophysi. J. 95(12), 5661-5680 (2008).
29. Thorne RG, Nicholson C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl Acad. Sci. U.S.A. 103(14), 5567-5572 (2006).
30. Seidel S, Garvalov BK, Wirta V et al. A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain 133(Pt 4), 983-995 (2010).
31. Miletic H, Niclou SP, Johansson M, Bjerkvig R. Anti-VEGF therapies for malignant glioma: treatment effects and escape mechanisms. Expert Opin. Ther. Targets 13(4), 455-468 (2009).
32. Weiler M, Blaes J, Pusch S et al. mTOR target NDRG1 confers MGMT-dependent resistance to alkylating chemotherapy. Proc. Natl Acad. Sci. U.S.A. 111(1), 409-414 (2014).
33. Prados, Michael D: Neuro-oncology The Essentials., M Bernstein, MS Berger (Eds). Thieme, NY, USA. (2008)..
34. Cheung HC, Hai T, Zhu W et al. Splicing factors PTBP1 and PTBP2 promote proliferation and migration of glioma cell lines. Brain 132(Pt 8), 2277-2288 (2009).
35. Eisele G, Wischhusen J, Mittelbronn M et al. TGF-beta and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells. Brain 129(Pt 9), 2416-2425 (2006).
36. Rao RD, Mladek AC, Lamont JD et al. Disruption of parallel and converging signaling pathways contributes to the synergistic antitumor effects of simultaneous mTOR and EGFR inhibition in GBM cells. Neoplasia 7(10), 921-929 (2005).
37. Christensen BC, Smith AA, Zheng S et al. DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma. J. Natl Cancer Inst. 103(2), 143-53 (2011).
38. Clarke J, Penas C, Pastori C et al. Epigenetic pathways and glioblastoma treatment. Epigenetics 8(8), 785-795 (2013).
39. Niola F, Zhao X, Singh D et al. Mesenchymal high-grade glioma is maintained by the ID-RAP1 axis. J. Clin. Invest. 123(1), 405 (2013).
40. Tso CL, Shintaku P, Chen J et al. Primary glioblastomas express mesenchymal stem-like properties. Mol. Cancer Res. 4(9), 607-619 (2006).
41. Hemmati HD, Nakano I, Lazareff JA et al. Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl Acad. Sci. U.S.A. 100(25), 15178-15183 (2003).
42. Mischel PS, Cloughesy TF, Nelson SF. DNA-microarray analysis of brain cancer: molecular classification for therapy. Nat. Rev. Neurosci. 5(10), 782-792 (2004).
43. Tabatabai G, Bähr O, Möhle R et al. Lessons from the bone marrow: how malignant glioma cells attract adult haematopoietic progenitor cells. Brain 128(9), 2200-2211 (2005).
44. Tabatabai G, Herrmann C, Von Kurthy G et al. VEGF-dependent induction of CD62E on endothelial cells mediates glioma tropism of adult haematopoietic progenitor cells. Brain 131(Pt 10), 2579-2595 (2008).
45. Jin X, Kim SH, Jeon HM et al. Interferon regulatory factor 7 regulates glioma stem cells via interleukin-6 and Notch signalling. Brain 135(Pt 4), 1055-1069 (2012).
46. Fujita M, Scheurer ME, Decker SA et al. Role of type 1 IFNs in antiglioma immunosurveillance - using mouse studies to guide examination of novel prognostic markers in humans. Clin. Cancer Res. 16(13), 3409-3419 (2010).
47. Mesnil M, Yamasaki H. Bystander effect in herpes simplex virus-thymidine kinase/ganciclovir cancer gene therapy: role of gap-junctional intercellular communication. Cancer Res. 60(15), 3989-3999 (2000).
48. Trepel M, Stoneham CA, Eleftherohorinou H et al. A heterotypic bystander effect for tumor cell killing after adeno-associated virus/phage-mediated, vascular-targeted suicide gene transfer. Mol. Cancer Ther. 8(8), 2383-2391 (2009).
49. 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. 65(3), 279-289 (2003).
50. 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. 10(5), 967-972 (2004).
51. Izquierdo M, Martin V, De Felipe P et al. Human malignant brain tumor response to herpes simplex thymidine kinase (HSVtk)/ganciclovir gene therapy. Gen. Ther. 3(6), 491-495 (1996).
52. Klatzmann D, Valery CA, Bensimon G et al. A phase I/II study of herpes simplex virus type 1 thymidine kinase "suicide" gene therapy for recurrent glioblastoma. Study Group on Gene Therapy for Glioblastoma. Hum. Gene Ther. 9(17), 2595-2604 (1998).
53. Palu G, Cavaggioni A, Calvi P et al. Gene therapy of glioblastoma multiforme via combined expression of suicide and cytokine genes: a pilot study in humans. Gen. Ther. 6(3), 330-337 (1999).
54. Prados MD, Mcdermott M, Chang SM et al. Treatment of progressive or recurrent glioblastoma multiforme in adults with herpes simplex virus thymidine kinase gene vector-producer cells followed by intravenous ganciclovir administration: a phase I/II multi-institutional trial. J. Neurooncol. 65(3), 269-278 (2003).
55. Ram Z, Culver KW, Oshiro EM et al. Therapy of malignant brain tumors by intratumoral implantation of retroviral vector-producing cells. Nat. Med. 3(12), 1354-1361 (1997).
56. 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. 11(16), 2197-2205 (2000).
57. Shand N, Weber F, Mariani L et al. A phase 1-2 clinical trial of gene therapy for recurrent glioblastoma multiforme by tumor transduction with the herpes simplex thymidine kinase gene followed by ganciclovir. GLI328 European-Canadian Study Group. Hum. Gene Ther. 10(14), 2325-2335 (1999).
58. Smitt PS, Driesse M, Wolbers J, Kros M, Avezaat C. Treatment of relapsed malignant glioma with an adenoviral vector containing the herpes simplex thymidine kinase gene followed by ganciclovir. Mol. Ther. 7(6), 851-858 (2003).
59. Trask TW, Trask RP, Aguilar-Cordova E et al. Phase I study of adenoviral delivery of the HSV-tk gene and ganciclovir administration in patients with current malignant brain tumors. Mol. Ther. 1(2), 195-203 (2000).
60. Packer RJ, Raffel C, Villablanca JG et al. Treatment of progressive or recurrent pediatric malignant supratentorial brain tumors with herpes simplex virus thymidine kinase gene vector-producer cells followed by intravenous ganciclovir administration. J. Neurosurg. 92(2), 249-254 (2000).
61. Rainov NG. A phase III clinical evaluation of herpes simplex virus type 1 thymidine kinase and ganciclovir gene therapy as an adjuvant to surgical resection and radiation in adults with previously untreated glioblastoma multiforme. Hum. Gene Ther. 11(17), 2389-2401 (2000).
62. Westphal M, Yla-Herttuala S, Martin J et al. Adenovirus-mediated gene therapy with sitimagene ceradenovec followed by intravenous ganciclovir for patients with operable high-grade glioma (ASPECT): a randomised, open-label, phase 3 trial. Lancet Oncol. 14(9), 823-833 (2013).
63. Culver KW, Ram Z, Wallbridge S, Ishii H, Oldfield EH, Blaese RM. In vivo gene transfer with retroviral vector-producer cells for treatment of experimental brain tumors. Science 256(5063), 1550-1552 (1992).
64. Huang KC, Altinoz M, Wosik K et al. Impact of the coxsackie and adenovirus receptor (CAR) on glioma cell growth and invasion: requirement for the C-terminal domain. Int. J. Cancer 113(5), 738-745 (2005).
65. Clapham PR, McKnight A. Cell surface receptors, virus entry and tropism of primate lentiviruses. J. Gen. Virol. 83(Pt 8), 1809-1829 (2002).
66. Asaoka K, Tada M, Sawamura Y, Ikeda J, Abe H. Dependence of efficient adenoviral gene delivery in malignant glioma cells on the expression levels of the Coxsackievirus and adenovirus receptor. J. Neurosurg. 92(6), 1002-1008 (2000).
67. Jimenez T, Fox WP, Naus CC, Galipeau J, Belliveau DJ. Connexin over-expression differentially suppresses glioma growth and contributes to the bystander effect following HSV-thymidine kinase gene therapy. Cell Commun. Adhes. 13(1-2), 79-92 (2006).
68. Garcia-Rodriguez L, Perez-Torras S, Carrio M et al. Connexin-26 is a key factor mediating gemcitabine bystander effect. Mol. Cancer Ther. 10(3), 505-517 (2011).
69. Sanson M, Marcaud V, Robin E, Valery C, Sturtz F, Zalc B. Connexin 43-mediated bystander effect in two rat glioma cell models. Cancer Gene Ther. 9(2), 149-155 (2002).
70. Yu SC, Xiao HL, Jiang XF et al. Connexin 43 reverses malignant phenotypes of glioma stem cells by modulating E-cadherin. Stem Cells 30(2), 108-120 (2012).
71. Lin JH, Takano T, Cotrina ML et al. Connexin 43 enhances the adhesivity and mediates the invasion of malignant glioma cells. J. Neurosci. 22(11), 4302-4311 (2002).
72. Sin WC, Crespin S, Mesnil M. Opposing roles of connexin43 in glioma progression. Biochim. Biophys. Acta 1818(8), 2058-2067 (2012).
73. Ostertag D, Amundson KK, Lopez Espinoza F et al. Brain tumor eradication and prolonged survival from intratumoral conversion of 5-fluorocytosine to 5-fluorouracil using a nonlytic retroviral replicating vector. Neuro-oncology 14(2), 145-159 (2012).
74. 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. 21(13), 2508-2518 (2003).
75. Mineta T, Rabkin SD, Yazaki T, Hunter WD, Martuza RL. Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas. Nat. Med. 1(9), 938-943 (1995).
76. Liu BL, Robinson M, Han ZQ et al. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene Ther. 10(4), 292-303 (2003).
77. Montgomery RI, Warner MS, Lum BJ, Spear PG. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87(3), 427-436 (1996).
78. Zhou G, Roizman B. Characterization of a recombinant herpes simplex virus 1 designed to enter cells via the IL13Ralpha2 receptor of malignant glioma cells. J. Virol. 79(9), 5272-5277 (2005).
79. Kesari S, Randazzo BP, Valyi-Nagy T et al. Therapy of experimental human brain tumors using a neuroattenuated herpes simplex virus mutant. Lab. Invest. 73(5), 636-648 (1995).
80. Markert JM, Liechty PG, Wang W et al. Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol. Ther. 17(1), 199-207 (2009).
81. Markert JM, Medlock MD, Rabkin SD et al. Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther. 7(10), 867-874 (2000).
82. Papanastassiou V, Rampling R, Fraser M et al. The potential for efficacy of the modified (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Ther. 9(6), 398-406 (2002).
83. Rampling R, Cruickshank G, Papanastassiou V et al. Toxicity evaluation of replication-competent herpes simplex virus (ICP 34.5 null mutant 1716) in patients with recurrent malignant glioma. Gene Ther. 7(10), 859-866 (2000).
84. Lorence RM, Katubig BB, Reichard KW et al. Complete regression of human fibrosarcoma xenografts after local Newcastle disease virus therapy. Cancer Res. 54(23), 6017-6021 (1994).
85. Csatary LK, Bakacs T. Use of Newcastle disease virus vaccine (MTH-68/H) in a patient with high-grade glioblastoma. JAMA 281(17), 1588-1589 (1999).
86. Csatary LK, Gosztonyi G, Szeberenyi J et al. MTH-68/H oncolytic viral treatment in human high-grade gliomas. J. Neurooncol. 67(1-2), 83-93 (2004).
87. Freeman AI, Zakay-Rones Z, Gomori JM et al. Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. Mol. Ther. 13(1), 221-228 (2006).
88. Forsyth P, Roldan G, George D et al. A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. Mol. Ther. 16(3), 627-632 (2008).
89. Kicielinski KP, Chiocca EA, Yu JS, Gill GM, Coffey M, Markert JM. Phase I Clinical Trial of Intratumoral Reovirus Infusion for the Treatment of Recurrent Malignant Gliomas in Adults. Mol. Ther.22(5), 1056-1062 (2014).
90. 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. 10(5), 958-966 (2004).
91. Gomez-Manzano C, Fueyo J. Oncolytic adenoviruses for the treatment of brain tumors. Curr. Opin. Mol. Ther. 12(5), 530-537 (2010).
92. Ylosmaki E, Hakkarainen T, Hemminki A, Visakorpi T, Andino R, Saksela K. Generation of a conditionally replicating adenovirus based on targeted destruction of E1A mRNA by a cell type-specific MicroRNA. J. Virol. 82(22), 11009-11015 (2008).
93. Alonso MM, Gomez-Manzano C, Bekele BN, Yung WK, Fueyo J. Adenovirus-based strategies overcome temozolomide resistance by silencing the O6-methylguanine-DNA methyltransferase promoter. Cancer Res. 67(24), 11499-11504 (2007).
94. Roulstone V, Twigger K, Zaidi S et al. Synergistic cytotoxicity of oncolytic reovirus in combination with cisplatin-paclitaxel doublet chemotherapy. Gene Ther. 20(5), 521-528 (2013).
95. Wakabayashi T, Natsume A, Hashizume Y, Fujii M, Mizuno M, Yoshida J. A phase I clinical trial of interferon-beta gene therapy for high-grade glioma: novel findings from gene expression profiling and autopsy. J. Gene Med. 10(4), 329-339 (2008).
96. Yoshida J, Mizuno M, Fujii M et al. Human gene therapy for malignant gliomas (glioblastoma multiforme and anaplastic astrocytoma) by in vivo transduction with human interferon beta gene using cationic liposomes. Hum. Gene Ther. 15(1), 77-86 (2004).
97. Chiocca EA, Smith KM, Mckinney B et al. A phase I trial of Ad.hIFN-beta gene therapy for glioma. Mol. Ther. 16(3), 618-626 (2008).
98. Asavarut P, Zhao H, Gu J, Ma D. The role of HMGB1 in inflammation-mediated organ injury. Acta Anaesthesiol. Taiwan 51(1), 28-33 (2013).
99. Candolfi M, Yagiz K, Foulad D et al. Release of HMGB1 in response to proapoptotic glioma killing strategies: efficacy and neurotoxicity. Clin. Cancer Res. 15(13), 4401-4414 (2009).
100. Curtin JF, Liu N, Candolfi M et al. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med. 6(1), e10 (2009).
101. Wurdinger T, Tannous BA. Glioma angiogenesis: Towards novel RNA therapeutics. Cell Adh. Migr. 3(2), 230-235 (2009).
102. Gondi CS, Lakka SS, Dinh DH, Olivero WC, Gujrati M, Rao JS. Downregulation of uPA, uPAR and MMP-9 using small, interfering, hairpin RNA (siRNA) inhibits glioma cell invasion, angiogenesis and tumor growth. Neuron Glia Biol. 1(2), 165-176 (2004).
103. Lakka SS, Gondi CS, Yanamandra N et al. Inhibition of cathepsin B and MMP-9 gene expression in glioblastoma cell line via RNA interference reduces tumor cell invasion, tumor growth and angiogenesis. Oncogene 23(27), 4681-4689 (2004).
104. Purow BW, Haque RM, Noel MW et al. Expression of Notch-1 and its ligands, Delta-like-1 and Jagged-1, is critical for glioma cell survival and proliferation. Cancer Res. 65(6), 2353-2363 (2005).
105. Jensen SA, Day ES, Ko CH et al. Spherical nucleic acid nanoparticle conjugates as an RNAi-based therapy for glioblastoma. Sci. Transl. Med. 5(209), 209ra152 (2013).
106. Chen Y, Zhu X, Zhang X, Liu B, Huang L. Nanoparticles modified with tumor-targeting scFv deliver siRNA and miRNA for cancer therapy. Mol. Ther. 18(9), 1650-1656 (2010).
107. Gondi CS, Lakka SS, Yanamandra N et al. Expression of antisense uPAR and antisense uPA from a bicistronic adenoviral construct inhibits glioma cell invasion, tumor growth, and angiogenesis. Oncogene 22(38), 5967-5975 (2003).
108. Saydam O, Glauser DL, Heid I et al. Herpes simplex virus 1 amplicon vector-mediated siRNA targeting epidermal growth factor receptor inhibits growth of human glioma cells in vivo. Mol. Ther. 12(5), 803-812 (2005).
109. Andrews DW, Resnicoff M, Flanders AE et al. Results of a pilot study involving the use of an antisense oligodeoxynucleotide directed against the insulin-like growth factor type I receptor in malignant astrocytomas. J. Clin. Oncol. 19(8), 2189-2200 (2001).
110. Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin. Microbiol. Rev. 21(4), 583-593 (2008).
111. Aslanidi G, Lamb K, Zolotukhin S. An inducible system for highly efficient production of recombinant adeno-associated virus (rAAV) vectors in insect Sf9 cells. Proc. Natl Acad. Sci. U.S.A. 106(13), 5059-5064 (2009).
112. Kotin RM. Large-scale recombinant adeno-associated virus production. Hum. Mol. Genet. 20(R1), R2-6 (2011).
113. Kaeppel C, Beattie SG, Fronza R et al. A largely random AAV integration profile after LPLD gene therapy. Nat. Med. 19(7), 889-891 (2013).
114. Donsante A, Miller DG, Li Y et al. AAV vector integration sites in mouse hepatocellular carcinoma. Science 317(5837), 477 (2007).
115. Kay MA, Nakai H. Looking into the safety of AAV vectors. Nature 424(6946), 251 (2003).
116. Grimm D, Pandey K, Nakai H, Storm TA, Kay MA. Liver transduction with recombinant adeno-associated virus is primarily restricted by capsid serotype not vector genotype. J. Virol. 80(1), 426-439 (2006).
117. Wang L, Wang H, Bell P et al. Systematic evaluation of AAV vectors for liver directed gene transfer in murine models. Mol. Ther. 18(1), 118-125 (2010).
118. Wang B, Li J, Fu FH et al. Construction and analysis of compact muscle-specific promoters for AAV vectors. Gene Ther. 15(22), 1489-1499 (2008).
119. Phillips MI, Tang Y, Schmidt-Ott K, Qian K, Kagiyama S. Vigilant vector: heart-specific promoter in an adeno-associated virus vector for cardioprotection. Hypertension 39(2 Pt 2), 651-655 (2002).
120. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol. Ther. 16(6), 1073-1080 (2008).
121. Jooss K, Chirmule N. Immunity to adenovirus and adeno-associated viral vectors: implications for gene therapy. Gene Ther. 10(11), 955-963 (2003).
122. Rabinowitz JE, Rolling F, Li C et al. Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J. Virol. 76(2), 791-801 (2002).
123. Grimm D, Lee JS, Wang L et al. In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J. Virol. 82(12), 5887-5911 (2008).
124. White SJ, Nicklin SA, Buning H et al. Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 109(4), 513-519 (2004).
125. Work LM, Buning H, Hunt E et al. Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses. Mol. Ther. 13(4), 683-693 (2006).
126. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotech. 27(1), 59-65 (2009).
127. Ng SS, Gao Y, Chau DH et al. A novel glioblastoma cancer gene therapy using AAV-mediated long-term expression of human TERT C-terminal polypeptide. Cancer Gene Ther. 14(6), 561-572 (2007).
128. Okada H, Miyamura K, Itoh T et al. Gene therapy against an experimental glioma using adeno-associated virus vectors. Gene Ther. 3(11), 957-964 (1996).
129. Clackson T, Lowman HB. Phage Display: A Practical Approach. Oxford University Press, Oxford, UK (2004).
130. Smith GP. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228(4705), 1315-1317 (1985).
131. Bradbury AR, Sidhu S, Dubel S, Mccafferty J. Beyond natural antibodies: the power of in vitro display technologies. Nat. Biotech. 29(3), 245-254 (2011).
132. Pasqualini R, Ruoslahti E. Organ targeting in vivo using phage display peptide libraries. Nature 380(6572), 364-366 (1996). This key paper is the first report that shows the feasibility of using bacteriophages for targeting specific receptors or antigens in vivo.
133. Arap W, Kolonin MG, Trepel M et al. Steps toward mapping the human vasculature by phage display. Nat. Med. 8(2), 121-127 (2002).
134. Mintz PJ, Kim J, Do KA et al. Fingerprinting the circulating repertoire of antibodies from cancer patients. Nat. Biotech. 21(1), 57-63 (2003).
135. Pasqualini R, Koivunen E, Ruoslahti E. αv integrins as receptors for tumor targeting by circulating ligands. Nat. Biotech. 15(6), 542-546 (1997). A key study that identifies specific integrins that are expressed on angiogenic tumors and that form the basis of tumor targeting using the RGD4C ligand.
136. Jay SM, Lee RT. Protein engineering for cardiovascular therapeutics: untapped potential for cardiac repair. Circ. Res. 113(7), 933-943 (2013).
137. Nicklin SA, White SJ, Watkins SJ, Hawkins RE, Baker AH. Selective targeting of gene transfer to vascular endothelial cells by use of peptides isolated by phage display. Circulation 102(2), 231-237 (2000).
138. Zhang L, Hoffman JA, Ruoslahti E. Molecular profiling of heart endothelial cells. Circulation 112(11), 1601-1611 (2005).
139. Larocca D, Witte A, Johnson W, Pierce GF, Baird A. Targeting bacteriophage to mammalian cell surface receptors for gene delivery. Hum. Gene Ther. 9(16), 2393-2399 (1998). This paper is the first study that shows the feasibility of filamentous bacteriophage for delivering reporter genes to mammalian cells.
140. Burg MA, Jensen-Pergakes K, Gonzalez AM, Ravey P, Baird A, Larocca D. Enhanced phagemid particle gene transfer in camptothecin-treated carcinoma cells. Cancer Res. 62(4), 977-981 (2002).
141. Larocca D, Jensen-Pergakes K, Burg MA, Baird A. Receptor-targeted gene delivery using multivalent phagemid particles. Mol. Ther. 3(4), 476-484 (2001).
142. Larocca D, Kassner PD, Witte A, Ladner RC, Pierce GF, Baird A. Gene transfer to mammalian cells using genetically targeted filamentous bacteriophage. FASEB J. 13(6), 727-734 (1999).
143. Poul MA, Marks JD. Targeted gene delivery to mammalian cells by filamentous bacteriophage. J. Mol. Biol. 288(2), 203-211 (1999).
144. Urbanelli L, Ronchini C, Fontana L, Menard S, Orlandi R, Monaci P. Targeted gene transduction of mammalian cells expressing the HER2/neu receptor by filamentous phage. J. Mol. Biol. 313(5), 965-976 (2001).
145. Hajitou A, Rangel R, Trepel M et al. Design and construction of targeted AAVP vectors for mammalian cell transduction. Nat. Protoc. 2(3), 523-531 (2007).
146. Hajitou A, Trepel M, Lilley CE et al. A hybrid vector for ligand-directed tumor targeting and molecular imaging. Cell 125(2), 385-398 (2006). This is a key study that characterizes the hybrid adeno-associated virus/phage vector for targeted systemic gene delivery and molecular imaging.
147. Kia A, Przystal JM, Nianiaris N, Mazarakis ND, Mintz PJ, Hajitou A. Dual systemic tumor targeting with ligand-directed phage and Grp78 promoter induces tumor regression. Mol. Cancer Ther. 11(12), 2566-2577 (2012).
148. Arap MA, Lahdenranta J, Mintz PJ et al. Cell surface expression of the stress response chaperone GRP78 enables tumor targeting by circulating ligands. Cancer Cell 6(3), 275-284 (2004).
149. Brooks PC, Clark RA, Cheresh DA. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264(5158), 569-571 (1994).
150. Chatterjee S, Matsumura A, Schradermeier J, Gillespie GY. Human malignant glioma therapy using anti-alpha(v)beta3 integrin agents. J. Neurooncol. 46(2), 135-144 (2000).
151. Gladson CL, Cheresh DA. Glioblastoma expression of vitronectin and the alpha v beta 3 integrin. Adhesion mechanism for transformed glial cells. J. Clin. Invest. 88(6), 1924-1932 (1991).
152. Koutsioumpa M, Polytarchou C, Courty J et al. Interplay between alphavbeta3 integrin and nucleolin regulates human endothelial and glioma cell migration. J. Biol. Chem. 288(1), 343-354 (2013).
153. Schnell O, Krebs B, Carlsen J et al. Imaging of integrin alpha(v)beta(3) expression in patients with malignant glioma by [18F] Galacto-RGD positron emission tomography. Neuro-oncology 11(6), 861-870 (2009).
154. Hajitou A, Pasqualini R, Arap W. Vascular targeting: recent advances and therapeutic perspectives. Trends Cardiovasc. Med. 16(3), 80-88 (2006).
155. Tandle A, Hanna E, Lorang D et al. Tumor vasculature-targeted delivery of tumor necrosis factor-alpha. Cancer 115(1), 128-139 (2009).
156. Przystal JM, Umukoro E, Stoneham CA et al. Proteasome inhibition in cancer is associated with enhanced tumor targeting by the adeno-associated virus/phage. Mol. Oncol. 7(1), 55-66 (2013).
157. Stoneham CA, Hollinshead M, Hajitou A. Clathrin-mediated Endocytosis and Subsequent Endo-Lysosomal Trafficking of Adeno-associated Virus/Phage. J. Biol. Chem. 287(43), 35849-35859 (2012).
158. Kia A, Yata T, Hajji N, Hajitou A. Inhibition of Histone Deacetylation and DNA Methylation Improves Gene Expression Mediated by the Adeno-Associated Virus/Phage in Cancer Cells. Viruses 5(10), 2561-2572 (2013).
159. Soghomonyan S, Hajitou A, Rangel R et al. Molecular PET imaging of HSV1-tk reporter gene expression using [18F] FEAU. Nat. Protoc. 2(2), 416-423 (2007).
160. Hajitou A, Lev DC, Hannay JaF et al. A preclinical model for predicting drug response in soft-tissue sarcoma with targeted AAVP molecular imaging. Proc. Natl Acad. Sci. 105(11), 4471-4476 (2008). The findings of this study report the potential of using adeno-associated virus/phage vectors for translational and diagnostic applications.
161. Paoloni MC, Tandle A, Mazcko C et al. Launching a novel preclinical infrastructure: comparative oncology trials consortium directed therapeutic targeting of TNFalpha to cancer vasculature. PloS ONE 4(3), e4972 (2009).