Development of adenovirus capsid proteins for targeted therapeutic delivery

Therapeutic Delivery

Volumn 4, Issue 2, 2013, Pages 267-277

  Medina Kauwe, Lali K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; DOXORUBICIN; DOXORUBICIN DERIVATIVE; FIBER PROTEIN; HERDOX; HERGA; HEXON PROTEIN; PENTON BASE PROTEIN; RECOMBINANT PENTON BASE PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADENOVIRUS INFECTION; ANTINEOPLASTIC ACTIVITY; BINDING AFFINITY; CELL FUNCTION; COMPETITIVE INHIBITION; DRUG ACCUMULATION; DRUG APPROVAL; DRUG CYTOTOXICITY; DRUG PROTEIN BINDING; DRUG TARGETING; ELECTRON MICROSCOPY; ENDOCYTOSIS; FLUORESCENCE ANALYSIS; GENE EXPRESSION; HUMAN; INTERCALATION COMPLEX; INTRACELLULAR TRANSPORT; LOW DRUG DOSE; MOLECULAR INTERACTION; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PARTICLE SIZE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; REVIEW; SOLID TUMOR; VIRUS CAPSID; VIRUS ENTRY; VIRUS MORPHOLOGY;

EID: 84872920980     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.12.155     Document Type: Review

References (80)

1. Van Oostrum J, Smith PR, Mohraz M, Burnett RM. The structure of the adenovirus capsid. III. Hexon packing determined from electron micrographs of capsid fragments. J. Mol. Biol. 198(1), 73-89 (1987).
2. Echavarria M. Adenoviruses in immunocompromised hosts. Clin. Microbiol. Rev. 21(4), 704-715 (2008).
3. Medina-Kauwe LK. Endocytosis of adenovirus and adenovirus capsid proteins. Adv. Drug Deliv. Rev. 55(11), 1485-1496 (2003).
4. Boudin ML, Boulanger P. Assembly of adenovirus penton base and fiber. Virology 116(2), 589-604 (1982).
5. Shayakhmetov DM, Lieber A. Dependence of adenovirus infectivity on length of the fiber shaft domain. J. Virol. 74(22), 10274-10286 (2000).
6. Van Raaij MJ, Mitraki A, Lavigne G, Cusack S. A triple beta-spiral in the adenovirus fibre shaft reveals a new structural motif for a fibrous protein. Nature 401(6756), 935-938 (1999).
7. Bergelson JM, Cunningham JA, Droguett G et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275(5304), 1320-1323 (1997).
8. Roelvink PW, Lizonova A, Lee JG et al. The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J. Virol. 72(10), 7909-7915 (1998).
9. Xia D, Henry LJ, Gerard RD, Deisenhofer J. Crystal structure of the receptor-binding domain of adenovirus type 5 fiber protein at 1.7 A resolution. Structure 2(12), 1259-1270 (1994).
10. 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 286(5444), 1579-1583 (1999).
11. Cohen CJ, Shieh JT, Pickles RJ, Okegawa T, Hsieh JT, Bergelson JM. The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction. Proc. Natl Acad. Sci. USA 98(26), 15191-15196 (2001).
12. Medina-Kauwe LK, Chen X. Using GFP-ligand fusions to measure receptor-mediated endocytosis in living cells. In: Vitamins and Hormones, Litwack G (Ed.). Elsevier Science, San Diego, CA, USA 81-95 (2002).
13. Medina-Kauwe LK, Leung V, Wu L, Kedes L. Assessing the binding and endocytosis activity of cellular receptors using GFP-ligand fusions. BioTechniques 29, 602-609 (2000).
14. Rentsendorj A, Agadjanian H, Chen X et al. The Ad5 fiber mediates nonviral gene transfer in the absence of the whole virus, utilizing a novel cell entry pathway. Gene Ther. 12(3), 225-237. (2005).
15. Gaggar A, Shayakhmetov DM, Lieber A. CD46 is a cellular receptor for group B adenoviruses. Nat. Med. 9(11), 1408-1412 (2003).
16. Lenaerts L, Van Dam W, Persoons L, Naesens L. Interaction between mouse adenovirus type 1 and cell surface heparan sulfate proteoglycans. PLoS ONE 7(2), e31454 (2012).
17. Xie J, Chiang L, Contreras J et al. Novel fiber-dependent entry mechanism for adenovirus serotype 5 in lacrimal acini. J. Virol. 80(23), 11833-11851 (2006).
18. Bayo-Puxan N, Cascallo M, Gros A, Huch M, Fillat C, Alemany R. Role of the putative heparan sulfate glycosaminoglycan-binding site of the adenovirus type 5 fiber shaft on liver detargeting and knob-mediated retargeting. J. Gene Virol. 87(Pt 9), 2487-2495 (2006).
19. Wang H, Li ZY, Liu Y et al. Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nat. Med. 17(1), 96-104 (2011).
20. Stewart PL, Fuller SD, Burnett RM. Difference imaging of adenovirus: bridging the resolution gap between x-ray crystallography and electron microscopy. EMBO. J. 12(7), 2589-2599 (1993).
21. Zubieta C, Schoehn G, Chroboczek J, Cusack S. The structure of the human adenovirus 2 penton. Mol. Cell 17(1), 121-135. (2005).
22. Chiu CY, Mathias P, Nemerow GR, Stewart PL. Structure of adenovirus complexed with its internalization receptor, alphavbeta5 integrin. J. Virol. 73(8), 6759-6768 (1999).
23. Rentsendorj A, Xie J, Macveigh M et al. Typical and atypical trafficking pathways of Ad5 penton base recombinant protein: implications for gene transfer. Gene Ther. 13(10), 821-836. (2006).
24. Parker AL, Waddington SN, Nicol CG et al. Multiple vitamin K-dependent coagulation zymogens promote adenovirus-mediated gene delivery to hepatocytes. Blood 108(8), 2554-2561 (2006).
25. Kalyuzhniy O, Di Paolo NC, Silvestry M et al. Adenovirus serotype 5 hexon is critical for virus infection of hepatocytes in vivo. Proc. Natl Acad. Sci. USA 105(14), 5483-5488 (2008).
26. Waddington SN, Mcvey JH, Bhella D et al. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 132(3), 397-409 (2008).
27. Meier O, Boucke K, Hammer SV et al. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158(6), 1119-1131 (2002).
28. Meier O, Greber UF. Adenovirus endocytosis. J. Gene Med. 6(Suppl 1), S152-S163. (2004).
29. Nakano MY, Boucke K, Suomalainen M, Stidwill RP, Greber UF. The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J. Virol. 74(15), 7085-7095 (2000).
30. Greber UF, Willetts M, Webster P, Helenius A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75(3), 477-486 (1993).
31. Seth P. Adenovirus-dependent release of choline from plasma membrane vesicles at an acidic pH is mediated by the penton base protein. J. Virol. 68(2), 1204-1206 (1994).
32. Seth P, Willingham MC, Pastan I. Binding of adenovirus and its external proteins to Triton X-114. Dependence on pH. J. Biol. Chem. 260(27), 14431-14434 (1985).
33. Wang K, Guan T, Cheresh DA, Nemerow GR. Regulation of adenovirus membrane penetration by the cytoplasmic tail of integrin beta5. J. Virol. 74(6), 2731-2739 (2000).
34. Wickham TJ, Filardo EJ, Cheresh DA, Nemerow GR. Integrin alpha v beta 5 selectively promotes adenovirus mediated cell membrane permeabilization. J. Cell Biol. 127(1), 257-264 (1994).
35. Cotten M, Weber JM. The adenovirus protease is required for virus entry into host cells. Virology 213(2), 494-502 (1995).
36. Greber UF, Webster P, Weber J, Helenius A. The role of the adenovirus protease on virus entry into cells. EMBO J. 15(8), 1766-1777 (1996).
37. Miyazawa N, Crystal RG, Leopold PL. Adenovirus serotype 7 retention in a late endosomal compartment prior to cytosol escape is modulated by fiber protein. J. Virol. 75(3), 1387-1400 (2001).
38. Miyazawa N, Leopold PL, Hackett NR et al. Fiber swap between adenovirus subgroups B and C alters intracellular trafficking of adenovirus gene transfer vectors. J. Virol. 73(7), 6056-6065 (1999).
39. Seth P, Fitzgerald D, Ginsberg H, Willingham M, Pastan I. Evidence that the penton base of adenovirus is involved in potentiation of toxicity of Pseudomonas exotoxin conjugated to epidermal growth factor. Mol. Cell. Biol. 4(8), 1528-1533 (1984).
40. Wiethoff CM, Wodrich H, Gerace L, Nemerow GR. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol 79(4), 1992-2000 (2005).
41. Hong SS, Gay B, Karayan L, Dabauvalle MC, Boulanger P. Cellular uptake and nuclear delivery of recombinant adenovirus penton base. Virology. 262(1), 163-177. (1999).
42. Prchla E, Plank C, Wagner E, Blaas D, Fuchs R. Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J. Cell Biol. 131(1), 111-123 (1995).
43. Kelkar S, De BP, Gao G, Wilson JM, Crystal RG, Leopold PL. A common mechanism for cytoplasmic dynein-dependent microtubule binding shared among adeno-associated virus and adenovirus serotypes. J Virol. 80(15), 7781-7785 (2006).
44. Kelkar SA, Pfister KK, Crystal RG et al. Cytoplasmic dynein mediates adenovirus binding to microtubules. J. Virol. 78(18), 10122-10132 (2004).
45. Leopold PL, Kreitzer G, Miyazawa N et al. Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis. Hum. Gene Ther. 11(1), 151-165 (2000).
46. Karayan L, Hong SS, Gay B, Tournier J, D'angeac AD, Boulanger P. Structural and functional determinants in adenovirus type 2 penton base recombinant protein. J. Virol. 71(11), 8678-8689 (1997).
47. Medina-Kauwe LK, Maguire M, Kasahara N, Kedes L. Non-viral gene delivery to human breast cancer cells by targeted Ad5 penton proteins. Gene Ther. 8, 1753-1761 (2001).
48. Fender P, Ruigrok RW, Gout E, Buffet S, Chroboczek J. Adenovirus dodecahedron, a new vector for human gene transfer. Nature Biotechnol. 15(1), 52-56 (1997).
49. Szolajska E, Burmeister WP, Zochowska M et al. The structural basis for the integrity of Adenovirus Ad3 dodecahedron. PLoS ONE 7(9), e46075 (2012).
50. Vives RR, Lortat-Jacob H, Chroboczek J, Fender P. Heparan sulfate proteoglycan mediates the selective attachment and internalization of serotype 3 human adenovirus dodecahedron. Virology 321(2), 332-340 (2004).
51. Fender P, Schoehn G, Perron-Sierra F, Tucker GC, Lortat-Jacob H. Adenovirus dodecahedron cell attachment and entry are mediated by heparan sulfate and integrins and vary along the cell cycle. Virology 371(1), 155-164 (2008).
52. Gout E, Schoehn G, Fenel D, Lortat-Jacob H, Fender P. The adenovirus type 3 dodecahedron's RGD loop comprises an HSPG binding site that influences integrin binding. J. Biomed. Biotechnol. 541939 (2010) (2010).
53. Fuschiotti P, Schoehn G, Fender P et al. Structure of the dodecahedral penton particle from human adenovirus type 3. J. Mol. Biol. 356(2), 510-520 (2006).
54. Schoehn G, Fender P, Chroboczek J, Hewat EA. Adenovirus 3 penton dodecahedron exhibits structural changes of the base on fibre binding. EMBO J. 15(24), 6841-6846 (1996).
55. Galinier R, Gout E, Lortat-Jacob H, Wood J, Chroboczek J. Adenovirus protein involved in virus internalization recruits ubiquitin-protein ligases. Biochemistry 41(48), 14299-14305 (2002).
56. Garcel A, Gout E, Timmins J, Chroboczek J, Fender P. Protein transduction into human cells by adenovirus dodecahedron using WW domains as universal adaptors. J. Gene Med. 8(4), 524-531 (2006).
57. Zochowska M, Paca A, Schoehn G et al. Adenovirus dodecahedron, as a drug delivery vector. PLoS ONE 4(5), e5569 (2009).
58. Medina-Kauwe LK, Kasahara N, Kedes L. 3PO, a novel non-viral gene delivery system using engineered Ad5 penton proteins. Gene Ther. 8, 795-803 (2001).
59. Agadjanian H, Ma J, Rentsendorj A et al. Tumor detection and elimination by a targeted gallium corrole. Proc. Natl Acad. Sci. USA 106(15), 6105-6110 (2009).
60. Agadjanian H, Weaver JJ, Mahammed A et al. Specific delivery of corroles to cells via noncovalent conjugates with viral proteins. Pharm. Res. 23(2), 367-377 (2006).
61. Rentsendorj A, Agadjanian H, Chen H et al. The Ad5 fiber mediates non-viral gene transfer in the absence of the whole virus, utilizing a novel cell entry pathway. Gene Ther. 12(3), 225-237 (2005).
62. Sepp-Lorenzino L, Eberhard I, Ma Z et al. Signal transduction pathways induced by heregulin in MDA-MB-453 breast cancer cells. Oncogene 12(8), 1679-1687 (1996).
63. Goldman R, Levy RB, Peles E, Yarden Y. Heterodimerization of the ErbB-1 and ErbB-2 receptors in human breast carcinoma cells: a mechanism for receptor transregulation. Biochemistry 29(50), 11024-11028 (1990).
64. Sliwkowski MX, Schaefer G, Akita RW et al. Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 269(20), 14661-14665 (1994).
65. Medina-Kauwe LK. Non-viral mediated gene delivery for therapeutic applications. In: Gene Therapy for Neurological Disorders. Lowenstein P, Castro M (Eds). Informa Healthcare, London, UK, 115-140 (2006).
66. Martin ME, Rice KG. Peptide-guided gene delivery. AAPS J. 9(1), E18-E29 (2007).
67. Agadjanian H, Chu D, Hwang JY et al. Chemotherapy targeting by DNA capture in viral protein particles. Nanomedicine 7(3), 335-352 (2012).
68. Hwang JY, Park J, Kang BJ et al. Multimodality imaging in vivo for preclinical assessment of tumor-targeted doxorubicin nanoparticles. PLoS ONE 7(4), e34463 (2012).
69. Gross Z, Galili N, Saltsman I. The first direct synthesis of corroles from pyrrole. Angew. Chem. Int. Ed. Engl. 38, 1427-1429 (1999).
70. Mahammed A, Gray HB, Weaver JJ, Sorasaenee K, Gross Z. Amphiphilic corroles bind tightly to human serum albumin. Bioconjug. Chem. 15, 738-746 (2004).
71. Hwang JY, Lubow J, Chu D et al. Photoexcitation of tumor-targeted corrole induces singlet oxygen-mediated augmentation of cytotoxicity. J.Release 163(3), 368-373 (2012).
72. Hwang JY, Lubow J, Chu D et al. A mechanistic study of tumor-targeted corrole toxicity. Mol. Pharm. 8(6), 2233-2243 (2011).
73. Hwang JY, Lubow J, Gray HB et al. Investigating photoexcitation-induced mitochondrial damage by chemotherapeutic corroles using multimode optical imaging. J. Biomed. Opt. (2012) (In Press).
74. Hwang JY, Wachsmann-Hogiu S, Ramanujan VK et al. A multimode optical imaging system for preclinical applications in vivo: technology development, multiscale imaging, and chemotherapy assessment. Mol. Imaging Biol. 14(4), 431-432(2011).
75. Bradley RR, Lynch DM, Iampietro MJ, Borducchi EN, Barouch DH. Adenovirus serotype 5 neutralizing antibodies target both hexon and fiber following vaccination and natural infection. J. Virol. 86(1), 625-629 (2012).
76. Sun G, Hsueh PY, Janib SM, Hamm-Alvarez S, Mackay JA. Design and cellular internalization of genetically engineered polypeptide nanoparticles displaying adenovirus knob domain. J. Control. Release 155(2), 218-226 (2011).
77. Carlisle RC, Bettinger T, Ogris M, Hale S, Mautner V, Seymour LW. Adenovirus hexon protein enhances nuclear delivery and increases transgene expression of polyethylenimine/plasmid DNA vectors. Mol. Ther. 4(5), 473-483 (2001).
78. Greber UF, Suomalainen M, Stidwill RP, Boucke K, Ebersold MW, Helenius A. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16(19), 5998-6007 (1997).
79. Pollard H, Toumaniantz G, Amos JL et al. Ca2+-sensitive cytosolic nucleases prevent efficient delivery to the nucleus of injected plasmids. J. Gene Med. 3(2), 153-164 (2001).
80. Lukacs GL, Haggie P, Seksek O, Lechardeur D, Freedman N, Verkman AS. Size-dependent DNA mobility in cytoplasm and nucleus. J. Biol. Chem. 275(3), 1625-1629 (2000).