Enhanced central nervous system transduction with lentiviral vectors pseudotyped with RVG/HIV-1gp41 chimeric envelope glycoproteins

Journal of Virology

Volumn 88, Issue 5, 2014, Pages 2877-2890

  Trabalza, Antonio ^a   Eleftheriadou, Ioanna ^a   Sgourou, Argyro ^b   Liao, Ting Yi ^a   Patsali, Petros ^a   Lee, Heyne ^a   Mazarakis, Nicholas D ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b HELLENIC OPEN UNIVERSITY   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GLYCOPROTEIN GP 41; LENTIVIRUS VECTOR; LYTIC PEPTIDE 2; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CORPUS STRIATUM; GENE TRANSFER; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; RABIES; RABIES VIRUS; SIGNAL TRANSDUCTION;

BRAIN; CELL LINE; CENTRAL NERVOUS SYSTEM; DOPAMINERGIC NEURONS; GENE EXPRESSION; GENETIC VECTORS; HEK293 CELLS; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; LENTIVIRUS; PLASMIDS; RECOMBINANT FUSION PROTEINS; TRANSDUCTION, GENETIC; VIRAL ENVELOPE PROTEINS; VIRAL LOAD;

EID: 84896725749     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03376-13     Document Type: Article

References (50)

1. Canivet M, Hoffman AD, Hardy D, Sernatinger J, Levy JA. 1990. Replication of HIV-1 in a wide variety of animal cells following phenotypic mixing with murine retroviruses. Virology 178:543-551. http://dx .doi.org/10.1016/0042-6822(90)90352-R.
2. Chesebro B, Wehrly K, Maury W. 1990. Differential expression in human and mouse cells of human immunodeficiency virus pseudotyped by murine retroviruses. J. Virol. 64:4553-4557.
3. Lusso P, di Marzo Veronese F, Ensoli B, Franchini G, Jemma C, DeRocco SE, Kalyanaraman VS, Gallo RC. 1990. Expanded HIV-1 cellular tropism by phenotypic mixing with murine endogenous retroviruses. Science 247:848-852. http://dx.doi.org/10.1126/science.2305256.
4. Spector DH, Wade E, Wright DA, Koval V, Clark C, Jaquish D, Spector SA. 1990. Human immunodeficiency virus pseudotypes with expanded cellular and species tropism. J. Virol. 64:2298-2308.
5. Zhu ZH, Chen SS, Huang AS. 1990. Phenotypic mixing between human immunodeficiency virus and vesicular stomatitis virus or herpes simplex virus. J. Acquir. Immune Defic. Syndr. 3:215-219.
6. Cronin J, Zhang XY, Reiser J. 2005. Altering the tropism of lentiviral vectors through pseudotyping. Curr. Gene Ther. 5:387-398. http://dx.doi .org/10.2174/1566523054546224.
7. Bartz SR, Rogel ME, Emerman M. 1996. Human immunodeficiency virus type 1 cell cycle control: Vpr is cytostatic and mediates G2 accumulation by a mechanism which differs from DNA damage checkpoint control. J. Virol. 70:2324-2331.
8. Mazarakis ND, Azzouz M, Rohll JB, Ellard FM, Wilkes FJ, Olsen AL, Carter EE, Barber RD, Baban DF, Kingsman SM, Kingsman AJ, O'Malley K, Mitrophanous KA. 2001. Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum. Mol. Genet. 10:2109-2121. http://dx.doi.org/10.1093/hmg/10.19.2109.
9. Mitrophanous K, Yoon S, Rohll J, Patil D, Wilkes F, Kim V, Kingsman S, Kingsman A, Mazarakis N. 1999. Stable gene transfer to the nervous system using a non-primate lentiviral vector. Gene Ther. 6:1808-1818. http://dx.doi.org/10.1038/sj.gt.3301023.
10. Wong LF, Azzouz M, Walmsley LE, Askham Z, Wilkes FJ, Mitrophanous KA, Kingsman SM, Mazarakis ND. 2004. Transduction patterns of pseudotyped lentiviral vectors in the nervous system. Mol. Ther. 9:101-111. http://dx.doi.org/10.1016/j.ymthe.2003.09.017.
11. Mentis GZ, Gravell M, Hamilton R, Shneider NA, O'Donovan MJ, Schubert M. 2006. Transduction of motor neurons and muscle fibers by intramuscular injection of HIV-1-based vectors pseudotyped with select rabies virus glycoproteins. J. Neurosci. Methods 157:208-217. http://dx .doi.org/10.1016/j.jneumeth.2006.04.011.
12. Kato S, Inoue K, Kobayashi K, Yasoshima Y, Miyachi S, Inoue S, Hanawa H, Shimada T, Takada M, Kobayashi K. 2007. Efficient gene transfer via retrograde transport in rodent and primate brains using a human immunodeficiency virus type 1-based vector pseudotyped with rabies virus glycoprotein. Hum. Gene Ther. 18:1141-1151. http://dx.doi .org/10.1089/hum.2007.082.
13. Federici T, Kutner R, Zhang XY, Kuroda H, Tordo N, Boulis NM, Reiser J. 2009. Comparative analysis of HIV-1-based lentiviral vectors bearing lyssavirus glycoproteins for neuronal gene transfer. Genet. Vaccines Ther. 7:1. http://dx.doi.org/10.1186/1479-0556-7-1.
14. Mochizuki H, Schwartz JP, Tanaka K, Brady RO, Reiser J. 1998. High-titer human immunodeficiency virus type 1-based vector systems for gene delivery into nondividing cells. J. Virol. 72:8873-8883.
15. Zingler K, Littman DR. 1993. Truncation of the cytoplasmic domain of the simian immunodeficiency virus envelope glycoprotein increases Env incorporation into particles and fusogenicity and infectivity. J. Virol. 67: 2824-2831.
16. Kato S, Kobayashi K, Inoue K, Kuramochi M, Okada T, Yaginuma H, Morimoto K, Shimada T, Takada M, Kobayashi K. 2011. A lentiviral strategy for highly efficient retrograde gene transfer by pseudotyping with fusion envelope glycoprotein. Hum. Gene Ther. 22:197-206. http://dx.doi .org/10.1089/hum.2009.179.
17. Carpentier DC, Vevis K, Trabalza A, Georgiadis C, Ellison SM, Asfahani RI, Mazarakis ND. 2012. Enhanced pseudotyping efficiency of HIV-1 lentiviral vectors by a rabies/vesicular stomatitis virus chimeric envelope glycoprotein. Gene Ther. 19:761-774. http://dx.doi.org/10.1038/gt.2011 .124.
18. Funke S, Schneider IC, Glaser S, Muhlebach MD, Moritz T, Cattaneo R, Cichutek K, Buchholz CJ. 2009. Pseudotyping lentiviral vectors with the wild-type measles virus glycoproteins improves titer and selectivity. Gene Ther. 16:700-705. http://dx.doi.org/10.1038/gt.2009.11.
19. Funke S, Maisner A, Muhlebach MD, Koehl U, Grez M, Cattaneo R, Cichutek K, Buchholz CJ. 2008. Targeted cell entry of lentiviral vectors. Mol. Ther. 16:1427-1436. http://dx.doi.org/10.1038/mt.2008.128.
20. Checkley MA, Luttge BG, Freed EO. 2011. HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J. Mol. Biol. 410:582-608. http://dx.doi.org/10.1016/j.jmb.2011.04.042.
21. Murakami T, Freed EO. 2000. Genetic evidence for an interaction between human immunodeficiency virus type 1 matrix and alpha-helix 2 of the gp41 cytoplasmic tail. J. Virol. 74:3548-3554. http://dx.doi.org/10 .1128/JVI.74.8.3548-3554.2000.
22. Murakami T, Freed EO. 2000. The long cytoplasmic tail of gp41 is required in a cell type-dependent manner for HIV-1 envelope glycoprotein incorporation into virions. Proc. Natl. Acad. Sci. U.S.A. 97:343-348. http://dx.doi.org/10.1073/pnas.97.1.343.
23. Dubay JW, Roberts SJ, Hahn BH, Hunter E. 1992. Truncation of the human immunodeficiency virus type 1 transmembrane glycoprotein cytoplasmic domain blocks virus infectivity. J. Virol. 66:6616-6625.
24. Gabuzda DH, Lever A, Terwilliger E, Sodroski J. 1992. Effects of deletions in the cytoplasmic domain on biological functions of human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 66:3306-3315.
25. Yu X, Yuan X, McLane MF, Lee TH, Essex M. 1993. Mutations in the cytoplasmic domain of human immunodeficiency virus type 1 transmembrane protein impair the incorporation of Env proteins into mature virions. J. Virol. 67:213-221.
26. Freed EO, Martin MA. 1996. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 70:341-351.
27. Cosson P. 1996. Direct interaction between the envelope and matrix proteins of HIV-1. EMBO J. 15:5783-5788.
28. Wyma DJ, Kotov A, Aiken C. 2000. Evidence for a stable interaction of gp41 with Pr55(Gag) in immature human immunodeficiency virus type 1 particles. J. Virol. 74:9381-9387. http://dx.doi.org/10.1128/JVI.74.20 .9381-9387.2000.
29. Lu L, Zhu Y, Huang J, Chen X, Yang H, Jiang S, Chen YH. 2008. Surface exposure of the HIV-1 env cytoplasmic tail LLP2 domain during the membrane fusion process: interaction with gp41 fusion core. J. Biol. Chem. 283:16723-16731. http://dx.doi.org/10.1074/jbc.M801083200.
30. Miller MA, Garry RF, Jaynes JM, Montelaro RC. 1991. A structural correlation between lentivirus transmembrane proteins and natural cytolytic peptides. AIDS Res. Hum. Retroviruses 7:511-519. http://dx.doi.org /10.1089/aid.1991.7.511.
31. Deschambeault J, Lalonde JP, Cervantes-Acosta G, Lodge R, Cohen EA, Lemay G. 1999. Polarized human immunodeficiency virus budding in lymphocytes involves a tyrosine-based signal and favors cell-to-cell viral transmission. J. Virol. 73:5010-5017.
32. Zhu P, Chertova E, Bess J, Jr, Lifson JD, Arthur LO, Liu J, Taylor KA, Roux KH. 2003. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. U. S. A. 100:15812-15817. http://dx.doi.org/10.1073/pnas .2634931100.
33. Gaudin Y, Tuffereau C, Durrer P, Brunner J, Flamand A, Ruigrok R. 1999. Rabies virus-induced membrane fusion. Mol. Membr. Biol. 16:21-31. http://dx.doi.org/10.1080/096876899294724.
34. Chernomordik L, Chanturiya AN, Suss-Toby E, Nora E, Zimmerberg J. 1994. An amphipathic peptide from the C-terminal region of the human immunodeficiency virus envelope glycoprotein causes pore formation in membranes. J. Virol. 68:7115-7123.
35. Ean MA, Carruth LM, Rowell JF, Yu X, Siliciano RF. 1996. Human immunodeficiency virus type 1 envelope protein endocytosis mediated by a highly conserved intrinsic internalization signal in the cytoplasmic domain of gp41 is suppressed in the presence of the Pr55gag precursor protein. J. Virol. 70:6547-6556.
36. Hourioux C, Brand D, Sizaret PY, Lemiale F, Lebigot S, Barin F, Roingeard P. 2000. Identification of the glycoprotein 41(TM) cytoplasmic tail domains of human immunodeficiency virus type 1 that interact with Pr55Gag particles. AIDS Res. Hum. Retroviruses 16:1141-1147. http: //dx.doi.org/10.1089/088922200414983.
37. Freed EO, Martin MA. 1995. Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific, single amino acid substitutions in the human immunodeficiency virus type 1 matrix. J. Virol. 69:1984-1989.
38. Wyss S, Dimitrov AS, Baribaud F, Edwards TG, Blumenthal R, Hoxie JA. 2005. Regulation of human immunodeficiency virus type 1 envelope glycoprotein fusion by a membrane-interactive domain in the gp41 cytoplasmic tail. J. Virol. 79:12231-12241. http://dx.doi.org/10.1128/JVI.79 .19.12231-12241.2005.
39. Davis MR, Jiang J, Zhou J, Freed EO, Aiken C. 2006. A mutation in the human immunodeficiency virus type 1 Gag protein destabilizes the interaction of the envelope protein subunits gp120 and gp41. J. Virol. 80:2405-2417. http://dx.doi.org/10.1128/JVI.80.5.2405-2417.2006.
40. Wyma DJ, Jiang J, Shi J, Zhou J, Lineberger JE, Miller MD, Aiken C. 2004. Coupling of human immunodeficiency virus type 1 fusion to virion maturation: a novel role of the gp41 cytoplasmic tail. J. Virol. 78:3429-3435. http://dx.doi.org/10.1128/JVI.78.7.3429-3435.2004.
41. Murakami T, Ablan S, Freed EO, Tanaka Y. 2004. Regulation of human immunodeficiency virus type 1 Env-mediated membrane fusion by viral protease activity. J. Virol. 78:1026-1031. http://dx.doi.org/10.1128/JVI.78 .2.1026-1031.2004.
42. Byland R, Vance PJ, Hoxie JA, Marsh M. 2007. A conserved dileucine motif mediates clathrin and AP-2-dependent endocytosis of the HIV-1 envelope protein. Mol. Biol. Cell 18:414-425. http://dx.doi.org/10.1091 /mbc.E06-06-0535.
43. Wyss S, Berlioz-Torrent C, Boge M, Blot G, Honing S, Benarous R, Thali M. 2001. The highly conserved C-terminal dileucine motif in the cytosolic domain of the human immunodeficiency virus type 1 envelope glycoprotein is critical for its association with the AP-1 clathrin adaptor. J. Virol. 75:2982-2992. http://dx.doi.org/10.1128/JVI.75.6.2982-2992.2001.
44. Steckbeck JD, Sun C, Sturgeon TJ, Montelaro RC. 2010. Topology of the C-terminal tail of HIV-1 gp41: differential exposure of the Kennedy epitope on cell and viral membranes. PLoS One 5:e15261. http://dx.doi .org/10.1371/journal.pone.0015261.
45. Teixeira C, Gomes JR, Gomes P, Maurel F, Barbault F. 2011. Viral surface glycoproteins, gp120 and gp41, as potential drug targets against HIV-1: brief overview one quarter of a century past the approval of zidovudine, the first anti-retroviral drug. Eur. J. Med. Chem. 46:979-992. http://dx.doi.org/10.1016/j.ejmech.2011.01.046.
46. Hollier MJ, Dimmock NJ. 2005. The C-terminal tail of the gp41 transmembrane envelope glycoprotein of HIV-1 clades A, B, C, andDmay exist in two conformations: an analysis of sequence, structure, and function. Virology 337:284-296. http://dx.doi.org/10.1016/j.virol.2005.04.015.
47. Yang P, Ai LS, Huang SC, Li HF, Chan WE, Chang CW, Ko CY, Chen SS. 2010. The cytoplasmic domain of human immunodeficiency virus type 1 transmembrane protein gp41 harbors lipid raft association determinants. J. Virol. 84:59-75. http://dx.doi.org/10.1128/JVI.00899-09.
48. Schnell MJ, McGettigan JP, Wirblich C, Papaneri A. 2010. The cell biology of rabies virus: using stealth to reach the brain. Nat. Rev. Microbiol. 8:51-61. http://dx.doi.org/10.1038/nrmicro2260.
49. Edwards TG, Wyss S, Reeves JD, Zolla-Pazner S, Hoxie JA, Doms RW, Baribaud F. 2002. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein. J. Virol. 76:2683-2691. http://dx.doi.org/10 .1128/JVI.76.6.2683-2691.2002.
50. Cleveland SM, McLain L, Cheung L, Jones TD, Hollier M, Dimmock NJ. 2003. A region of the C-terminal tail of the gp41 envelope glycoprotein of human immunodeficiency virus type 1 contains a neutralizing epitope: evidence for its exposure on the surface of the virion. J. Gen. Virol. 84: 591-602. http://dx.doi.org/10.1099/vir.0.18630-0.