Retrovirus glycoprotein functionality requires proper alignment of the ectodomain and the membrane-proximal cytoplasmic tail

Journal of Virology

Volumn 87, Issue 23, 2013, Pages 12805-12813

  Janaka, Sanath Kumar ^a   Gregory, Devon A ^a   Johnson, Marc C ^a  

^a University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRIEND MURINE LEUKEMIA VIRUS ENVELOPE PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DELETION MUTANT; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; MICROENVIRONMENT; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; SEQUENCE ALIGNMENT; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS PARTICLE;

AMINO ACID SEQUENCE; CELL LINE; CELL MEMBRANE; CYTOPLASM; FRIEND MURINE LEUKEMIA VIRUS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RETROVIRIDAE INFECTIONS; SEQUENCE ALIGNMENT; VIRAL ENVELOPE PROTEINS; VIRUS ASSEMBLY;

EID: 84887174301     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01847-13     Document Type: Article

References (61)

1. Cronin J, Zhang XY, Reiser J. 2005. Altering the tropism of lentiviral vectors through pseudotyping. Curr. Gene Ther. 5:387-398.
2. Johnson MC. 2011. Mechanisms for Env glycoprotein acquisition by retroviruses. AIDS Res. Hum. Retroviruses 27:239-247.
3. Mazari PM, Roth MJ. 2013. Library screening and receptor-directed targeting of gammaretroviral vectors. Future Microbiol. 8:107-121.
4. Palù G, Parolin C, Takeuchi Y, Pizzato M. 2000. Progress with retroviral gene vectors. Rev. Med. Virol. 10:185-202.
5. Arce F, Breckpot K, Collins M, Escors D. 2011. Targeting lentiviral vectors for cancer immunotherapy. Curr. Cancer Ther. Rev. 7:248-260.
6. Desmaris N, Bosch A, Salaün C, Petit C, Prévost MC, Tordo N, Perrin P, Schwartz O, de Rocquigny H, Heard JM. 2001. Production and neurotropism of lentivirus vectors pseudotyped with lyssavirus envelope glycoproteins. Mol. Ther. 4:149-156.
7. Hachiya A, Sriwiriyanont P, Patel A, Saito N, Ohuchi A, Kitahara T, Takema Y, Tsuboi R, Boissy RE, Visscher MO, Wilson JM, Kobinger GP. 2007. Gene transfer in human skin with different pseudotyped HIV-based vectors. Gene Ther. 14:648-656.
8. Kato S, Kuramochi M, Takasumi K, Kobayashi K, Inoue K, Takahara D, Hitoshi S, Ikenaka K, Shimada T, Takada M, Kobayashi K. 2011. Neuron-specific gene transfer through retrograde transport of lentiviral vector pseudotyped with a novel type of fusion envelope glycoprotein. Hum. Gene Ther. 22:1511-1523.
9. Palomares K, Vigant F, Van Handel B, Pernet O, Chikere K, Hong P, Sherman SP, Patterson M, An DS, Lowry WE, Mikkola HK, Morizono K, Pyle AD, Lee B. 2013. Nipah virus envelope-pseudotyped lentiviruses efficiently target ephrinB2-positive stem cell populations in vitro and bypass the liver sink when administered in vivo. J. Virol. 87:2094-2108.
10. Martin F, Neil S, Kupsch J, Maurice M, Cosset F, Collins M. 1999. Retrovirus targeting by tropism restriction to melanoma cells. J. Virol. 73:6923-6929.
11. Fass D, Harrison SC, Kim PS. 1996. Retrovirus envelope domain at 1.7 angstrom resolution. Nat. Struct. Biol. 3:465-469.
12. Johnston ER, Radke K. 2000. The SU and TM envelope protein subunits of bovine leukemia virus are linked by disulfide bonds, both in cells and in virions. J. Virol. 74:2930-2935.
13. Leamnson RN, Halpern MS. 1976. Subunit structure of the glycoprotein complex of avian tumor virus. J. Virol. 18:956-968.
14. Opstelten DJ, Wallin M, Garoff H. 1998. Moloney murine leukemia virus envelope protein subunits, gp70 and Pr15E, form a stable disulfide-linked complex. J. Virol. 72:6537-6545.
15. Pinter A, Fleissner E. 1977. The presence of disulfide-linked gp70-p15(E) complexes in AKR murine leukemia virus. Virology 83:417-422.
16. Pinter A, Lieman-Hurwitz J, Fleissner E. 1978. The nature of the association between the murine leukemia virus envelope proteins. Virology 91:345-351.
17. Henzy JE, Coffin JM. 2013. Betaretroviral envelope subunits are noncovalently associated and restricted to the mammalian class. J. Virol. 87:1937-1946.
18. Kowalski M, Potz J, Basiripour L, Dorfman T, Goh WC, Terwilliger E, Dayton A, Rosen C, Haseltine W, Sodroski J. 1987. Functional regions of the envelope glycoprotein of human immunodeficiency virus type 1. Science 237:1351-1355.
19. Hunter E. 1997. Viral entry and receptors, p 71-119. In Coffin JM, Hughes SH, Varmus HE (ed), Retroviruses. Cold Spring Harbor Lab Press, Cold Spring Harbor, NY. Search Google Scholar
20. Löving R, Li K, Wallin M, Sjöberg M, Garoff H. 2008. R-peptide cleavage potentiates fusion-controlling isomerization of the intersubunit disulfide in Moloney murine leukemia virus Env. J. Virol. 82:2594-2597.
21. Ragheb JA, Anderson WF. 1994. pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. J. Virol. 68:3220-3231.
22. Wallin M, Ekstrom M, Garoff H. 2004. Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J. 23:54-65.
23. Kubo Y, Tominaga C, Yoshii H, Kamiyama H, Mitani C, Amanuma H, Yamamoto N. 2007. Characterization of R peptide of murine leukemia virus envelope glycoproteins in syncytium formation and entry. Arch. Virol. 152:2169-2182.
24. Li M, Li ZN, Yao Q, Yang C, Steinhauer DA, Compans RW. 2006. Murine leukemia virus R peptide inhibits influenza virus hemagglutinin-induced membrane fusion. J. Virol. 80:6106-6114.
25. Rein A, Mirro J, Haynes JG, Ernst SM, Nagashima K. 1994. Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J. Virol. 68:1773-1781.
26. Taylor GM, Sanders DA. 2003. Structural criteria for regulation of membrane fusion and virion incorporation by the murine leukemia virus TM cytoplasmic domain. Virology 312:295-305.
27. Yang C, Compans RW. 1997. Analysis of the murine leukemia virus R peptide: delineation of the molecular determinants which are important for its fusion inhibition activity. J. Virol. 71:8490-8496.
28. Henderson LE, Sowder R, Copeland TD, Smythers G, Oroszlan S. 1984. Quantitative separation of murine leukemia virus proteins by reversed-phase high-pressure liquid chromatography reveals newly described gag and env cleavage products. J. Virol. 52:492-500.
29. Löving R, Wu SR, Sjöberg M, Lindqvist B, Garoff H. 2012. Maturation cleavage of the murine leukemia virus Env precursor separates the transmembrane subunits to prime it for receptor triggering. Proc. Natl. Acad. Sci. U. S. A. 109:7735-7740.
30. Gebhardt A, Bosch JV, Ziemiecki A, Friis RR. 1984. Rous sarcoma virus p19 and gp35 can be chemically crosslinked to high molecular weight complexes. An insight into virus assembly. J. Mol. Biol. 174:297-317.
31. Manrique JM, Affranchino JL, González SA. 2008. In vitro binding of simian immunodeficiency virus matrix protein to the cytoplasmic domain of the envelope glycoprotein. Virology 374:273-279.
32. 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.
33. Cosson P. 1996. Direct interaction between the envelope and matrix proteins of HIV-1. EMBO J. 15:5783-5788.
34. Chakrabarti L, Emerman M, Tiollais P, Sonigo P. 1989. The cytoplasmic domain of simian immunodeficiency virus transmembrane protein modulates infectivity. J. Virol. 63:4395-4403.
35. Jones DR, Suzuki K, Piller SC. 2002. A 100-amino acid truncation in the cytoplasmic tail of glycoprotein 41 in the reference HIV type 1 strain RF. AIDS Res. Hum. Retroviruses 18:513-517.
36. Kodama T, Burns DP, Kestler HW III, Daniel MD, Desrosiers RC. 1990. Molecular changes associated with replication of simian immunodeficiency virus in human cells. J. Med. Primatol. 19:431-437.
37. Kodama T, Wooley DP, Naidu YM, Kestler HW III, Daniel MD, Li Y, Desrosiers RC. 1989. Significance of premature stop codons in env of simian immunodeficiency virus. J. Virol. 63:4709-4714.
38. Shimizu H, Hasebe F, Tsuchie H, Morikawa S, Ushijima H, Kitamura T. 1992. Analysis of a human immunodeficiency virus type 1 isolate carrying a truncated transmembrane glycoprotein. Virology 189:534-546.
39. Shimizu H, Morikawa S, Yamaguchi K, Tsuchie H, Hachimori K, Ushijima H, Kitamura T. 1990. Shorter size of transmembrane glycoprotein of an HIV-1 isolate. AIDS 4:575-576.
40. Lucas TM, Lyddon TD, Grosse SA, Johnson MC. 2010. Two distinct mechanisms regulate recruitment of murine leukemia virus envelope protein to retroviral assembly sites. Virology 405:548-555.
41. Kothe DL, Decker JM, Li Y, Weng Z, Bibollet-Ruche F, Zammit KP, Salazar MG, Chen Y, Salazar-Gonzalez JF, Moldoveanu Z, Mestecky J, Gao F, Haynes BF, Shaw GM, Muldoon M, Korber BT, Hahn BH. 2007. Antigenicity and immunogenicity of HIV-1 consensus subtype B envelope glycoproteins. Virology 360:218-234.
42. Aloia AL, Duffy L, Pak V, Lee KE, Sanchez-Martinez S, Derse D, Heidecker G, Cornetta K, Rein A. 2013. A reporter system for replication-competent gammaretroviruses: the inGluc-MLV-DERSE assay. Gene Ther. 20:169-176.
43. Mazurov D, Ilinskaya A, Heidecker G, Lloyd P, Derse D. 2010. Quantitative comparison of HTLV-1 and HIV-1 cell-to-cell infection with new replication dependent vectors. PLoS Pathog. 6:e1000788. doi:10.1371/journal.ppat.1000788.
44. Lewis BC, Chinnasamy N, Morgan RA, Varmus HE. 2001. Development of an avian leukosis-sarcoma virus subgroup A pseudotyped lentiviral vector. J. Virol. 75:9339-9344.
45. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP. 1995. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. U. S. A. 92:7297-7301.
46. Chesebro B, Wehrly K, Nishio J, Perryman S. 1992. Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. J. Virol. 66:6547-6554.
47. Krementsov DN, Rassam P, Margeat E, Roy NH, Schneider-Schaulies J, Milhiet PE, Thali M. 2010. HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components. Traffic 11:1401-1414.
48. Ono A, Freed EO. 2001. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. U. S. A. 98:13925-13930.
49. Buchan DW, Ward SM, Lobley AE, Nugent TC, Bryson K, Jones DT. 2010. Protein annotation and modelling servers at University College London. Nucleic Acids Res. 38(Suppl 2):W563-W568.
50. Jones DT. 1999. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292:195-202.
51. Erlwein O, Buchholz C, Schnierle BS. 2003. The proline-rich region of the ecotropic Moloney murine leukaemia virus envelope protein tolerates the insertion of the green fluorescent protein and allows the generation of replication-competent virus. J. Gen. Virol. 84:369-373.
52. Rothenberg SM, Olsen MN, Laurent LC, Crowley RA, Brown PO. 2001. Comprehensive mutational analysis of the Moloney murine leukemia virus envelope protein. J. Virol. 75:11851-11862.
53. Wu BW, Lu J, Gallaher TK, Anderson WF, Cannon PM. 2000. Identification of regions in the Moloney murine leukemia virus SU protein that tolerate the insertion of an integrin-binding peptide. Virology 269:7-17.
54. Ng VL, Wood TG, Arlinghaus RB. 1982. Processing of the env gene products of Moloney murine leukaemia virus. J. Gen. Virol. 59:329-343.
55. Jorgenson RL, Vogt VM, Johnson MC. 2009. Foreign glycoproteins can be actively recruited to virus assembly sites during pseudotyping. J. Virol. 83:4060-4067.
56. Januszeski MM, Cannon PM, Chen D, Rozenberg Y, Anderson WF. 1997. Functional analysis of the cytoplasmic tail of Moloney murine leukemia virus envelope protein. J. Virol. 71:3613-3619.
57. Wyma DJ, Jing 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.
58. 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.
59. Gregory DA, Lyddon TD, Johnson MC. 2013. Multiple Gag domains contribute to selective recruitment of murine leukemia virus (MLV) Env to MLV virions. J. Virol. 87:1518-1527.
60. Miyauchi K, Curran AR, Long Y, Kondo N, Iwamoto A, Engelman DM, Matsuda Z. 2010. The membrane-spanning domain of gp41 plays a critical role in intracellular trafficking of the HIV envelope protein. Retrovirology 7:95.
61. Janaka SK, Lucas TM, Johnson MC. 2011. Sequences in gibbon ape leukemia virus envelope that confer sensitivity to HIV-1 accessory protein Vpu. J. Virol. 85:11945-11954.