Lentiviruses inefficiently incorporate human parainfluenza type 3 envelope proteins

Biotechnology and Bioengineering

Volumn 99, Issue 4, 2008, Pages 1016-1027

  Jung, Cindy ^a   Le Doux, Joseph M ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Gene therapy; Human parainfluenza virus type 3; Lentivirus; Polarized cells; Pseudotyping

Indexed keywords

CELLS; GENE EXPRESSION; GENE TRANSFER; PROTEINS; RNA;

GENE THERAPY; HUMAN PARAINFLUENZA; LENTIVIRUS; POLARIZED CELLS; PSEUDOTYPE LENTIVIRUSES; TRANSFECTED CELLS;

VIRUSES;

F PROTEIN; GLYCOPROTEIN; HN PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ARTICLE; CELL SURFACE; CODON; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LENTIVIRINAE; PARAINFLUENZA VIRUS 3; PROTEIN EXPRESSION; VIRUS INFECTION; VIRUS PARTICLE; WILD TYPE; CELL LINE; GENE VECTOR; GENETICS; HELA CELL; KIDNEY; METABOLISM; METHODOLOGY; PHYSIOLOGY; VIROLOGY; VIRUS CULTURE;

HUMAN PARAINFLUENZA VIRUS 3; LENTIVIRUS;

CELL LINE; GENETIC VECTORS; HELA CELLS; HUMANS; KIDNEY; PARAINFLUENZA VIRUS 3, BOVINE; TRANSFECTION; VIRAL ENVELOPE PROTEINS; VIRUS CULTIVATION;

EID: 39549123459     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.21622     Document Type: Article

References (69)

1. Anderson WF. 1998. Human gene therapy. Nature 392 (6679 Suppl): 25–30.
2. Andersson H, Barth BU, Ekstrom M, Garoff H. 1997. Oligomerization‐dependent folding of the membrane fusion protein of Semliki Forest virus. J Virol 71 (12): 9654–9663.
3. Bachrach E, Dreja H, Lin YL, Mettling C, Pinet V, Corbeau P, Piechaczyk M. 2005. Effects of virion surface gp120 density on infection by HIV‐1 and viral production by infected cells. Virology 332 (1): 418–429.
4. Barki‐Harrington L. 2004. Oligomerisation of angiotensin receptors: Novel aspects in disease and drug therapy. J Renin Angiotensin Aldosterone Syst 5 (2): 49–52.
5. Bose S, Malur A, Banerjee AK. 2001. Polarity of human parainfluenza virus type 3 infection in polarized human lung epithelial A549 cells: Role of microfilament and microtubule. J Virol 75 (4): 1984–1989.
6. Cantin R, Methot S, Tremblay MJ. 2005. Plunder and stowaways: Incorporation of cellular proteins by enveloped viruses. J Virol 79 (11): 6577–6587.
7. Chanock RM, Murphy BR, Collins PL. 2001. Parainfluenza viruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, editors. Fields virology, 4th edn. Philadelphia: Lippincott‐Raven Publishers.
8. Chen ST, Iida A, Guo L, Friedmann T, Yee JK. 1996. Generation of packaging cell lines for pseudotyped retroviral vectors of the G protein of vesicular stomatitis virus by using a modified tetracycline inducible system. Proc Natl Acad Sci USA 93 (19): 10057–10062.
9. Christodoulopoulos I, Cannon PM. 2001. Sequences in the cytoplasmic tail of the gibbon ape leukemia virus envelope protein that prevent its incorporation into lentivirus vectors. J Virol 75 (9): 4129–4138.
10. Collins PL, Chanock RM, McIntosh K. 1996. Parainfluenza viruses. In: Fields BN, Knipe DM, Howley PM, Chanock RM, Melnick JL, Monath TP, Roizman B, Straus SE, editors. Fields virology, 3rd edn. Philadelphia: Lippincott‐Raven Publishers. p 1205–1243.
11. Copreni E, Penzo M, Carrabino S, Conese M. 2004. Lentivirus‐mediated gene transfer to the respiratory epithelium: A promising approach to gene therapy of cystic fibrosis. Gene Ther 11 (Suppl 1): S67–S75.
12. Cosset FL, Takeuchi Y, Battini JL, Weiss RA, Collins MK. 1995. High‐titer packaging cells producing recombinant retroviruses resistant to human serum. J Virol 69 (12): 7430–7436.
13. Cosson P. 1996. Direct interaction between the envelope and matrix proteins of HIV‐1. EMBO J 15 (21): 5783–5788.
14. De Larco JE, Rapp UR, Todaro GJ. 1978. Cell surface receptors for ecotropic MuLV: Detection and tissue distributions of free receptors in vivo. Int J Cancer 21 (3): 356–360.
15. Elango N, Coligan JE, Jambou RC, Venkatesan S. 1986. Human parainfluenza type 3 virus hemagglutinin‐neuraminidase glycoprotein: Nucleotide sequence of mRNA and limited amino acid sequence of the purified protein. J Virol 57 (2): 481–489.
16. Evans LH, Morrison RP, Malik FG, Portis J, Britt WJ. 1990. A neutralizable epitope common to the envelope glycoproteins of ecotropic, polytropic, xenotropic, and amphotropic murine leukemia viruses. J Virol 64 (12): 6176–6183.
17. Ferrari S, Griesenbach U, Shiraki‐Iida T, Shu T, Hironaka T, Hou X, Williams J, Zhu J, Jeffery PK, Geddes DM, et al., 2004. A defective nontransmissible recombinant Sendai virus mediates efficient gene transfer to airway epithelium in vivo. Gene Ther 11 (22): 1659–1664.
18. 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 (3): 1984–1989.
19. 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 (1): 341–351.
20. Hammarstedt M, Garoff H. 2004. Passive and active inclusion of host proteins in human immunodeficiency virus type 1 gag particles during budding at the plasma membrane. J Virol 785 (11): 686–697.
21. Harlow E, Lane D. 1988. Storing and purifying antibodies. Antibodies: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. p 288–303.
22. Henriksson P, Pfeiffer T, Zentgraf H, Alke A, Bosch V. 1999. Incorporation of wild‐type and C‐terminally truncated human epidermal growth factor receptor into human immunodeficiency virus‐like particles: Insight into the processes governing glycoprotein incorporation into retroviral particles. J Virol 73 (11): 9294–9302.
23. 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 (12): 1141–1147.
24. Hu XL, Ray R, Compans RW. 1992. Functional interactions between the fusion protein and hemagglutinin‐neuraminidase of human parainfluenza viruses. J Virol 66 (3): 1528–1534.
25. Johnson LG, Olsen JC, Naldini L, Boucher RC. 2000. Pseudotyped human lentiviral vector‐mediated gene transfer to airway epithelia in vivo. Gene Ther 7 (7): 568–574.
26. Jung C, Grzybowski BN, Tong S, Cheng L, Compans RW, Le Doux JM. 2004. Lentiviral vectors pseudotyped with envelope glycoproteins derived from human parainfluenza virus type 3. Biotechnol Prog 20 (6): 1810–1816.
27. Kang Y, Stein CS, Heth JA, Sinn PL, Penisten AK, Staber PD, Ratliff KL, Shen H, Barker CK, Martins I, et al., 2002. In vivo gene transfer using a nonprimate lentiviral vector pseudotyped with Ross River Virus glycoproteins. J Virol 76 (18): 9378–9388.
28. Kavanaugh MP, Miller DG, Zhang W, Law W, Kozak SL, Kabat D, Miller AD. 1994. Cell‐surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus are inducible sodium‐dependent phosphate symporters. Proc Natl Acad Sci USA 91 (15): 7071–7075.
29. Kobayashi M, Iida A, Ueda Y, Hasegawa M. 2003. Pseudotyped lentivirus vectors derived from simian immunodeficiency virus SIVagm with envelope glycoproteins from paramyxovirus. J Virol 77 (4): 2607–2614.
30. Kobinger GP, Weiner DJ, Yu QC, Wilson JM. 2001. Filovirus‐pseudotyped lentiviral vector can efficiently and stably transduce airway epithelia in vivo. Nat Biotechnol 19 (3): 225–230.
31. Kolegraff K, Bostik P, Ansari AA. 2006. Characterization and role of lentivirus‐associated host proteins. Exp Biol Med (Maywood) 231 (3): 252–263.
32. Kowolik CM, Yee JK. 2002. Preferential transduction of human hepatocytes with lentiviral vectors pseudotyped by Sendai virus F protein. Mol Ther 5 (6): 762–769.
33. Lallos LB, Laal S, Hoxie JA, Zolla‐Pazner S, Bandres JC. 1999. Exclusion of HIV coreceptors CXCR4, CCR5, and CCR3 from the HIV envelope. AIDS Res Hum Retroviruses 15 (10): 895–897.
34. Lavillette D, Russell SJ, Cosset FL. 2001. Retargeting gene delivery using surface‐engineered retroviral vector particles. Curr Opin Biotechnol 12 (5): 461–466.
35. Liu SL, Halbert CL, Miller AD. 2004. Jaagsiekte sheep retrovirus envelope efficiently pseudotypes human immunodeficiency virus type 1‐based lentiviral vectors. J Virol 78 (5): 2642–2647.
36. Logan AC, Nightingale SJ, Haas DL, Cho GJ, Pepper KA, Kohn DB. 2004. Factors influencing the titer and infectivity of lentiviral vectors. Hum Gene Ther 15 (10): 976–988.
37. Medina MF, Kobinger GP, Rux J, Gasmi M, Looney DJ, Bates P, Wilson JM. 2003. Lentiviral vectors pseudotyped with minimal filovirus envelopes increased gene transfer in murine lung. Mol Ther 8 (5): 777–789.
38. Mijnes JD, van der Horst LM, van Anken E, Horzinek MC, Rottier PJ, de Groot RJ. 1996. Biosynthesis of glycoproteins E and I of feline herpesvirus: gE‐gI interaction is required for intracellular transport. J Virol 70 (8): 5466–5475.
39. 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 (8): 3548–3554.
40. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272 (5259): 263–267.
41. Nguyen DG, Booth A, Gould SJ, Hildreth JE. 2003. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem 278 (52): 52347–52354.
42. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for high‐expression transfectants with a novel eukaryotic vector. Gene 108 (2): 193–199.
43. Nydegger S, Foti M, Derdowski A, Spearman P, Thali M. 2003. HIV‐1 egress is gated through late endosomal membranes. Traffic 4 (12): 902–910.
44. Orenstein JM, Meltzer MS, Phipps T, Gendelman HE. 1988. Cytoplasmic assembly and accumulation of human immunodeficiency virus types 1 and 2 in recombinant human colony‐stimulating factor‐1‐treated human monocytes: An ultrastructural study. J Virol 62 (8): 2578–2586.
45. Owens RJ, Dubay JW, Hunter E, Compans RW. 1991. Human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells. Proc Natl Acad Sci USA 88 (9): 3987–3991.
46. Pelchen‐Matthews A, Kramer B, Marsh M. 2003. Infectious HIV‐1 assembles in late endosomes in primary macrophages. J Cell Biol 162 (3): 443–455.
47. Pickl WF, Pimentel‐Muinos FX, Seed B. 2001. Lipid rafts and pseudotyping. J Virol 75 (15): 7175–7183.
48. Piller SC, Dubay JW, Derdeyn CA, Hunter E. 2000. Mutational analysis of conserved domains within the cytoplasmic tail of gp41 from human immunodeficiency virus type 1: Effects on glycoprotein incorporation and infectivity. J Virol 74 (24): 11717–11723.
49. Prinster SC, Hague C, Hall RA. 2005. Heterodimerization of g protein‐coupled receptors: Specificity and functional significance. Pharmacol Rev 57 (3): 289–298.
50. Radosevich M, Ono SJ. 2004. MHC class II gene expression is not induced in HPIV3‐infected respiratory epithelial cells. Immunol Res 30 (2): 125–138.
51. Sandrin V, Cosset FL. 2006. Intracellular versus cell surface assembly of retroviral pseudotypes is determined by the cellular localization of the viral glycoprotein, its capacity to interact with Gag, and the expression of the Nef protein. J Biol Chem 281 (1): 528–542.
52. Sandrin V, Muriaux D, Darlix JL, Cosset FL. 2004. Intracellular trafficking of Gag and Env proteins and their interactions modulate pseudotyping of retroviruses. J Virol 78 (13): 7153–7164.
53. Sinn PL, Burnight ER, Hickey MA, Blissard GW, McCray PB, Jr. 2005a. Persistent gene expression in mouse nasal epithelia following feline immunodeficiency virus‐based vector gene transfer. J Virol 79 (20): 12818–12827.
54. Sinn PL, Burnight ER, Shen H, Fan H, McCray PB, Jr. 2005b. Inclusion of Jaagsiekte sheep retrovirus proviral elements markedly increases lentivirus vector pseudotyping efficiency. Mol Ther 11 (3): 460–469.
55. Sinn PL, Penisten AK, Burnight ER, Hickey MA, Williams G, McCoy DM, Mallampalli RK, McCray PB. 2005c. Gene transfer to respiratory epithelia with lentivirus pseudotyped with Jaagsiekte sheep retrovirus envelope glycoprotein. Hum Gene Ther 16 (4): 479–488.
56. Sinn PL, Sauter SL, McCray PB, Jr. 2005d. Gene therapy progress and prospects: Development of improved lentiviral and retroviral vectors—Design, biosafety, and production. Gene Ther 12 (14): 1089–1098.
57. Spriggs MK, Olmsted RA, Venkatesan S, Coligan JE, Collins PL. 1986. Fusion glycoprotein of human parainfluenza virus type 3: Nucleotide sequence of the gene, direct identification of the cleavage‐activation site, and comparison with other paramyxoviruses. Virology 152 (1): 241–251.
58. Tong S, Compans RW. 1999. Alternative mechanisms of interaction between homotypic and heterotypic parainfluenza virus HN and F proteins. J Gen Virol 80 (Pt 1): 107–115.
59. Ulloa F, Real FX. 2001. Differential distribution of sialic acid in alpha2, 3 and alpha2,6 linkages in the apical membrane of cultured epithelial cells and tissues. J Histochem Cytochem 49 (4): 501–510.
60. Wang G, Davidson BL, Melchert P, Slepushkin VA, van Es HH, Bodner M, Jolly DJ, McCray PB, Jr. 1998. Influence of cell polarity on retrovirus‐mediated gene transfer to differentiated human airway epithelia. J Virol 72 (12): 9818–9826.
61. Wang G, Sinn PL, McCray PB, Jr. 2000a. Development of retroviral vectors for gene transfer to airway epithelia. Curr Opin Mol Ther 2 (5): 497–506.
62. Wang G, Zabner J, Deering C, Launspach J, Shao J, Bodner M, Jolly DJ, Davidson BL, McCray PB, Jr. 2000b. Increasing epithelial junction permeability enhances gene transfer to airway epithelia In vivo. Am J Respir Cell Mol Biol 22 (2): 129–138.
63. Yi Y, Hahm SH, Lee KH. 2005. Retroviral gene therapy: Safety issues and possible solutions. Curr Gene Ther 5 (1): 25–35.
64. Yu X, Yuan X, Matsuda Z, Lee TH, Essex M. 1992. The matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions. J Virol 66 (8): 4966–4971.
65. Yuste E, Reeves JD, Doms RW, Desrosiers RC. 2004. Modulation of Env content in virions of simian immunodeficiency virus: Correlation with cell surface expression and virion infectivity. J Virol 78 (13): 6775–6785.
66. Yuste E, Johnson W, Pavlakis GN, Desrosiers RC. 2005. Virion envelope content, infectivity, and neutralization sensitivity of simian immunodeficiency virus. J Virol 79 (19): 12455–12463.
67. Zhang L, Bukreyev A, Thompson CI, Watson B, Peeples ME, Collins PL, Pickles RJ. 2005. Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. J Virol 79 (2): 1113–1124.
68. 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 (5): 2824–2831.
69. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. 1997. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15 (9): 871–875.