Sstr2A: A relevant target for the delivery of genes into human Glioblastoma cells using fiber-modified adenoviral vectors

Gene Therapy

Volumn 20, Issue 3, 2013, Pages 283-297

  Lecolle K ^a,b   Begard S ^a,b   Caillierez, R ^a,b   Demeyer, D ^a,b   Grellier, E ^a,b   Loyens, A ^a,b   Csaba, Z ^a   Beauvillain, J C ^a,b   D'Halluin, J C ^a   Baroncini, M ^a,b,c   Lejeune, J P ^b,c   Sharif, A ^a,b   Prevot V ^a,b,c   Dournaud, P ^a   Buee L ^a,b,c   Colin, M ^a,b  

^a INSERM   (France)

^b UNIV LILLE   (France)

^c LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; SOMATOSTATIN RECEPTOR 2; VIRUS FIBER PROTEIN;

ARTICLE; CANCER GRADING; ELECTRON MICROSCOPY; EX VIVO STUDY; GENE EXPRESSION; GENETIC TRANSFECTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; AMINO ACID SEQUENCE; ANIMALS; BRAIN NEOPLASMS; CAPSID PROTEINS; CELL LINE, TUMOR; CELL NUCLEUS; CHO CELLS; COXSACKIE AND ADENOVIRUS RECEPTOR-LIKE MEMBRANE PROTEIN; CRICETINAE; CRICETULUS; ENDOCYTOSIS; GENETIC THERAPY; GENETIC VECTORS; GLIOBLASTOMA; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; INTEGRINS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; RECEPTORS, SOMATOSTATIN; SOMATOSTATIN; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 84874771239     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2012.39     Document Type: Article

References (68)

1. Behin A, Hoang-Xuan K, Carpentier AF, Delattre JY. Primary brain tumours in adults. Lancet 2003; 361: 323-331.
2. Kroeger KM, Muhammad AK, Baker GJ, Assi H, Wibowo MK, Xiong W et al. Gene therapy and virotherapy: novel therapeutic approaches for brain tumors. Discov Med 2010; 10: 293-304.
3. Jakobsson J, Lundberg C. Lentiviral vectors for use in the central nervous system. Mol Ther 2006; 13: 484-493.
4. Hacein-Bey-Abina S, von Kalle C, Schmidt M, Le Deist F, Wulffraat N, McIntyre E et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2003; 348: 255-256.
5. Campos SK, Barry MA. Current advances and future challenges in adenoviral vector biology and targeting. Curr Gene Ther 2007; 7: 189-204.
6. Hendrie PC, Russell W. Gene targeting with viral vectors. Mol Ther 2005; 12: 9-17.
7. Russell WC. Adenoviruses: update on structure and function. J Gen Virol 2009; 90(Part 1): 1-20.
8. Roelvink PW, Mi Lee G, Einfeld DA, Kovesdi I, Wickham TJ. Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 1999; 286: 1568-1571.
9. Barnett BG, Crews CJ, Douglas JT. Targeted adenoviral vectors. Biochim Biophys Acta. 2002; 1575: 1-14.
10. Dechecchi MC, Melotti P, Bonizzato A, Santacatterina M, Chilosi M, Cabrini G. Heparan sulfate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5. J Virol 2001; 75: 8772-8780.
11. Sullivan DE, Dash S, Du H, Hiramatsu N, Aydin F, Kolls J et al. Liver-directed gene transfer in non-human primates. Hum Gene Ther 1997; 8: 1195-1206.
12. Leissner P, Legrand V, Schlesinger Y, Hadji DA, van Raaij M, Cusack S et al. Influence of adenoviral fiber mutations on viral encapsidation, infectivity and in vivo tropism. Gene Therapy 2001; 8: 49-57.
13. Alemany R, Curiel DT. CAR-binding ablation does not change biodistribution and toxicity of adenoviral vectors. Gene Therapy 2001; 8: 1347-1353.
14. Smith T, Idamakanti N, Kylefjord H, Rollence M, King L, Kaloss M et al. In vivo hepatic adenoviral gene delivery occurs independently of the coxsackievirusadenovirus receptor. Mol Ther 2002; 5: 770-779.
15. Parker AL, McVey JH, Doctor JH, Lopez-Franco O, Waddington SNHavenga MJ et al. Influence of coagulation factor zymogens on the infectivity of adenoviruses pseudotyped with fibers from subgroup D. J Virol 2007; 81: 3627-3631.
16. Shayakhmetov DM, Gaggar A, Ni S, Li ZY, Lieber A. Adenovirus binding to blood factors results in liver cell infection and hepatotoxicity. J Virol 2005; 79: 7478-7491.
17. Waddington SN, McVey JH, Bhella D, Parker AL, Barker K, Atoda H et al. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 2008; 132: 397-409.
18. Kalyuzhniy O, Di Paolo NC, Silvestry M, Hofherr SE, Barry MA, Stewart PL et al. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc Natl Acad Sci USA 2008; 105: 5483-5488.
19. Vigant F, Descamps D, Jullienne B, Esselin S, Connault E, Opolon P et al. Substitution of hexon hypervariable region 5 of adenovirus serotype 5 abrogates blood factor binding and limits gene transfer to liver. Mol Ther 2008; 16: 1474-1480.
20. Alba R, Bradshaw AC, Parker AL, Bhella D, Waddington SN, Nicklin SA et al. Identification of coagulation factor (F)X binding sites on the adenovirus serotype 5 hexon: effect of mutagenesis on FX interactions and gene transfer. Blood 2009; 114: 965-971.
21. Sharma A, Li X, Bangari DS, Mittal SK. Adenovirus receptors and their implications in gene delivery. Virus Res 2009; 143: 184-194.
22. Renaut L, Colin M, Leite JP, Benko M, D'Halluin JC. Abolition of hCAR-dependent cell tropism using fiber knobs of Atadenovirus serotypes. Virology 2004; 321: 189-204.
23. Roge'e S, Grellier E, Bernard C, Jouy N, Loyens A, Beauvillain JC et al. Influence of chimeric human-bovine fibers on adenoviral entry into liver cells and the antiviral immune response. Gene Therapy 2010; 17: 880-891.
24. Nandi S, Lesniak MS. Adenoviral virotherapy for malignant brain tumors. Expert Opin Biol Ther 2009; 9: 737-747.
25. Candolfi M, Curtin JF, Xiong WD, Kroeger KM, Liu C, Rentsendorj A et al. Effective high-capacity gutless adenoviral vectors mediate transgene expression in human glioma cells. Mol Ther 2006; 14: 371-381.
26. Wang W, Zhu NL, Chua J, Swenson S, Costa FK, Schmitmeier S et al. Retargeting of adenoviral vector using basic fibroblast growth factor ligand for malignant glioma gene therapy. J Neurosurg 2005; 103: 1058-1066.
27. 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 2000; 92: 1002-1008.
28. Grill J, Van Beusechem VW, Van Der Valk P, Dirven CM, Leonhart A, Pherai DS et al. Combined targeting of adenoviruses to integrins and epidermal growth factor receptors increases gene transfer into primary glioma cells and spheroids. Clin Cancer Res 2001; 7: 641-650.
29. Kim M, Zinn KR, Barnett BG, Sumerel LA, Krasnykh V, Curiel DT et al. The therapeutic efficacy of adenoviral vectors for cancer gene therapy is limited by a low level of primary adenovirus receptors on tumour cells. Eur J Cancer 2002; 38: 1917-1926.
30. van Beusechem VW, Grill J, Mastenbroek DC, Wickham TJ, Roelvink PW, Haisma HJ et al. Efficient and selective gene transfer into primary human brain tumors by using single-chain antibody-targeted adenoviral vectors with native tropism abolished. J Virol 2002; 76: 2753-2762.
31. Gupta V, Wang W, Sosnowski BA, Hofman FM, Chen TC. Fibroblast growth factor- 2-retargeted adenoviral vector for selective transduction of primary glioblastoma multiforme endothelial cells. Neurosurg Focus 2006; 20: E26.
32. Piao Y, Jiang H, Alemany R, Krasnykh V, Marini FC, Xu J et al. Oncolytic adenovirus retargeted to Delta-EGFR induces selective antiglioma activity. Cancer Gene Ther 2009; 16: 256-265.
33. Leja J, Yu D, Nilsson B, Gedda L, Zieba A, Hakkarainen T et al. Oncolytic adenovirus modified with somatostatin motifs for selective infection of neuroendocrine tumor cells. Gene Therapy 2011; 18: 1052-1062.
34. Mailly L, Renaut L, Rogee S, Grellier E, D'Halluin JC, Colin M. Improved gene delivery to B lymphocytes using a modified adenovirus vector targeting CD21. Mol Ther 2006; 14: 293-304.
35. Held-Feindt JKB, Forstreuter F, Mentlein R. Somatostatin receptors in gliomas. J Physiol Paris 2000; 94: 251-258.
36. Mentlein R, Held-Feindt J, Krisch B. Topology of the signal transduction of the G protein-coupled somatostatin receptor sst2 in human glioma cells. Cell Tissue Res 2001; 303: 27-34.
37. Krisch B, Feindt J, Mentlein R. Immunoelectronmicroscopic analysis of the ligand-induced internalization of the somatostatin receptor subtype 2 in cultured human glioma cells. J Histochem Cytochem 1998; 46: 1233-1242.
38. Colin M, Mailly L, Rogee S, D'Halluin JC. Efficient species C HAdV infectivity in plasmocytic cell lines using a clathrin-independent lipid raft/caveola endocytic route. Mol Ther 2005; 11: 224-236.
39. Cervia D, Bagnoli P. An update on somatostatin receptor signaling in native systems and new insights on their pathophysiology. Pharmacol Ther 2007; 116: 322-341.
40. Patel YC. Somatostatin and its receptor family. Front Neuroendocrinol.20: 157-198.
41. Csaba Z, Dournaud P. Cellular biology of somatostatin receptors. Neuropeptides 2001; 35: 1-23.
42. Vanetti M, Vogt G, Hollt V. The two isoforms of the mouse somatostatin receptor (mSSTR2A and mSSTR2B) differ in coupling efficiency to adenylate cyclase and in agonist-induced receptor desensitization. FEBS Lett 1993; 331: 260-266.
43. Renaut L, Bernard C, D'Halluin JC. A rapid and easy method for production and selection of recombinant adenovirus genomes. J Virol Methods 2002; 100: 121-131.
44. Devaux C, Caillet-Boudin ML, Jacrot B, Boulanger P. Crystallization, enzymatique cleavage, and the polarity of the ade'novirus type 2 fiber. Virology 1987; 161: 121-128.
45. Csaba Z, Lelouvier B, Viollet C, El Ghouzzi V, Toyama K, Videau C et al. Activated somatostatin type 2 receptors traffic in vivo in central neurons from dendrites to the trans Golgi before recycling. Traffic 2007; 8: 820-834.
46. Csaba Z, Simon A, Helboe L, Epelbaum J, Dournaud P. Targeting sst2A receptorexpressing cells in the rat hypothalamus through in vivo agonist stimulation: neuroanatomical evidence for a major role of this subtype in mediating somatostatin functions. Endocrinology 2003; 144: 1564-1573.
47. Rogee S, Grellier E, Bernard C, Loyens A, Beauvillain JC, D'Halluin JC et al. Intracellular trafficking of a fiber-modified adenovirus using lipid raft/caveolae endocytosis. Mol Ther 2007; 15: 1963-1972.
48. Boisgerault N, Tangy F, Gregoire M. New perspectives in cancer virotherapy: bringing the immune system into play. Immunotherapy 2010; 2: 185-199.
49. Rommelaere J, Geletneky K, Angelova AL, Daeffler L, Dinsart C, Kiprianova I et al. Oncolytic parvoviruses as cancer therapeutics. Cytokine Growth Factor Rev 2010; 21: 185-195.
50. Munch RC, Muhlebach MD, Schaser T, Kneissl S, Jost C, Pluckthun A et al. DARPins: an efficient targeting domain for lentiviral vectors. Mol Ther 2011; 19: 686-693.
51. Ayala Breton C, Barber GN, Russell S, Peng KW. Retargeting Vesicular Stomatitis virus using Measles virus envelope glycoproteins. Hum Gene Ther 2011.
52. White K, Buning H, Kritz A, Janicki H, McVey J, Perabo L et al. Engineering adenoassociated virus 2 vectors for targeted gene delivery to atherosclerotic lesions. Gene Therapy 2008; 15: 443-451.
53. Campadelli-Fiume G, De Giovanni C, Gatta V, Nanni P, Lollini PL, Menotti L. Rethinking herpes simplex virus: the way to oncolytic agents. Rev Med Virol 2011; 21: 213-226.
54. Cawood R, Chen HH, Carroll F, Bazan-Peregrino M, van Rooijen N, Seymour LW. Use of tissue-specific microRNA to control pathology of wild-type adenovirus without attenuation of its ability to kill cancer cells. PLoS Pathog 2009; 5: e1000440.
55. Kron MW, Espenlaub S, Engler T, Schirmbeck R, Kochanek S, Kreppel F. miRNA-mediated silencing in hepatocytes can increase adaptive immune responses to adenovirus vector-delivered transgenic antigens. Mol Ther 19: 1547- 1557.
56. Bewley MC, Springer K, Zhang YB, Freimuth P, Flanagan JM. Structural analysis of the mechanism of adenovirus binding to its human cellular receptor, CAR. Science 1999; 286: 1579-1583.
57. Chiu CY, Mathias P, Nemerow GR, Stewart PL. Structure of adenovirus complexed with its internalization receptor, alphavbeta5 integrin. J Virol 1999; 73: 6759-6768.
58. Kao YJ, Ghosh M, Schonbrunn A. Ligand-dependent mechanisms of sst2a receptor trafficking: role of site-specific phosphorylation and receptor activation in the actions of biased somatostatin agonists. Mol Endocrinol 2011; 25: 1040-1054.
59. Leopold PL, Ferris B, Grinberg I, Worgall S, Hackett NR, Crystal RG. Fluorescent virions: dynamic tracking of the pathway of adenoviral gene transfer vectors in living cells. Hum Gene Ther 1998; 9: 367-378.
60. Lelouvier B, Tamagno G, Kaindl AM, Roland A, Lelievre V, Le Verche V et al. Dynamics of somatostatin type 2A receptor cargoes in living hippocampal neurons. J Neurosci 2008; 28: 4336-4349.
61. Dournaud P, Boudin H, Schonbrunn A, Tannenbaum GS, Beaudet A Interrelationships between somatostatin sst2A receptors and somatostatin- containing axons in rat brain: evidence for regulation of cell surface receptors by endogenous somatostatin. J Neurosci 1998; 18: 1056-1071.
62. Csaba Z, Richichi C, Bernard V, Epelbaum J, Vezzani A, Dournaud P. Plasticity of somatostatin and somatostatin sst2A receptors in the rat dentate gyrus during kindling epileptogenesis. Eur J Neurosci 2004; 19: 2531-2538.
63. Csaba Z, Pirker S, Lelouvier B, Simon A, Videau C, Epelbaum J et al. Somatostatin receptor type 2 undergoes plastic changes in the human epileptic dentate gyrus. J Neuropathol Exp Neurol 2005; 64: 956-969.
64. Nayak S, Herzog RW. Progress and prospects: immune responses to viral vectors. Gene Therapy 2010; 17: 295-304.
65. Immonen A, Vapalahti M, Tyynela K, Hurskainen H, Sandmair A, Vanninen R 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.
66. Kleihues P, Burger PC, Collins VP, Newcomb EW, Ohgaki H, Cavenee WK. Pathology and genetics of tumours of the nervous system. Glioblastoma 2000 29-39.
67. Sharif A, Duhem-Tonnelle V, Allet C, Baroncini M, Loyens A, Kerr-Conte J et al. Differential erbB signaling in astrocytes from the cerebral cortex and the hypothalamus of the human brain. Glia 2009; 57: 362-379.
68. Mathis JM, Bhatia S, Khandelwal A, Kovesdi I, Lokitz SJ, Odaka Y et al. Genetic incorporation of human metallothionein into the adenovirus protein IX for non-invasive SPECT imaging. PLoS One 2011; 6: e16792.