Mutations in the Cytoplasmic Domain of Human Immunodeficiency Virus Type 1 Transmembrane Protein Impair the Incorporation of Env Proteins into Mature Virions

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 1993 Jan 1

PMID 8416370

Citations 85

Authors

X Yu

X Yuan

M F McLane

T H Lee

M Essex

Affiliations

Soon will be listed here.

Abstract

In-frame stop codons were introduced into the coding region of human immunodeficiency virus type 1 (HIV-1) transmembrane protein (gp41). Truncation of 147 amino acids from the carboxyl terminus of gp41 (TM709) significantly decreased the stability and cell surface expression of the viral Env proteins, while truncation of 104 amino acids (TM752) did not. Truncation of 43 or more amino acids from the carboxyl terminus of gp41 generated mutant viruses which were noninfectious in several human CD4+ T lymphoid cell lines and fresh peripheral blood mononuclear cells. Analysis of the noninfectious mutant virions revealed significantly reduced incorporation of the Env proteins compared with the wild-type virions. Comparable amounts of Env proteins were detected on the surfaces of wild-type- and TM752-transfected cells, suggesting that the structures of gp41 required for efficient incorporation of Env proteins were disrupted in mutant TM752. Truncation of the last 12 amino acids (TM844) from the carboxyl terminus of gp41 did not significantly affect the assembly and release of virions or the incorporation of Env proteins into mature virions. However, the TM844 virus had dramatically decreased infectivity compared with the wild-type virus. This suggests that the cytoplasmic domain of gp41 also plays a role in other steps of virus replication.

Citing Articles

Tryptophan-based motifs in the LLP3 Region of the HIV-1 envelope glycoprotein cytoplasmic tail direct trafficking to the endosomal recycling compartment and mediate particle incorporation.

Lerner G, Ding L, Spearman P bioRxiv. 2023; .

PMID: 37162911 PMC: 10168361. DOI: 10.1101/2023.04.28.538708.

Role of the HIV-1 envelope transmembrane domain in intracellular sorting.

Perrin J, Bary A, Vernay A, Cosson P BMC Cell Biol. 2018; 19(1):3.

PMID: 29544440 PMC: 5856207. DOI: 10.1186/s12860-018-0153-4.

The Envelope Cytoplasmic Tail of HIV-1 Subtype C Contributes to Poor Replication Capacity through Low Viral Infectivity and Cell-to-Cell Transmission.

Santos da Silva E, Mulinge M, Lemaire M, Masquelier C, Beraud C, Rybicki A PLoS One. 2016; 11(9):e0161596.

PMID: 27598717 PMC: 5012655. DOI: 10.1371/journal.pone.0161596.

HIV-1 Cell-Free and Cell-to-Cell Infections Are Differentially Regulated by Distinct Determinants in the Env gp41 Cytoplasmic Tail.

Durham N, Chen B J Virol. 2015; 89(18):9324-37.

PMID: 26136566 PMC: 4542346. DOI: 10.1128/JVI.00655-15.

RRE-dependent HIV-1 Env RNA effects on Gag protein expression, assembly and release.

Lopez C, Sloan R, Cylinder I, Kozak S, Kabat D, Barklis E Virology. 2014; 462-463:126-34.

PMID: 24971705 PMC: 4125522. DOI: 10.1016/j.virol.2014.05.019.

References

Shimizu H, Hasebe F, Tsuchie H, Morikawa S, Ushijima H, Kitamura T . Analysis of a human immunodeficiency virus type 1 isolate carrying a truncated transmembrane glycoprotein. Virology. 1992; 189(2):534-46. DOI: 10.1016/0042-6822(92)90577-c. View

Suomalainen M, Garoff H . Alphavirus spike-nucleocapsid interaction and network antibodies. J Virol. 1992; 66(8):5106-9. PMC: 241379. DOI: 10.1128/JVI.66.8.5106-5109.1992. View

Guyader M, Emerman M, Sonigo P, Clavel F, Montagnier L, Alizon M . Genome organization and transactivation of the human immunodeficiency virus type 2. Nature. 1987; 326(6114):662-9. DOI: 10.1038/326662a0. View

Hirsch V, Riedel N, Mullins J . The genome organization of STLV-3 is similar to that of the AIDS virus except for a truncated transmembrane protein. Cell. 1987; 49(3):307-19. DOI: 10.1016/0092-8674(87)90283-2. View

Paabo S, Bhat B, Wold W, Peterson P . A short sequence in the COOH-terminus makes an adenovirus membrane glycoprotein a resident of the endoplasmic reticulum. Cell. 1987; 50(2):311-7. PMC: 7133293. DOI: 10.1016/0092-8674(87)90226-1. View

Chakrabarti L, Guyader M, Alizon M, Daniel M, Desrosiers R, Tiollais P . Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses. Nature. 1987; 328(6130):543-7. DOI: 10.1038/328543a0. View

Perez L, Davis G, Hunter E . Mutants of the Rous sarcoma virus envelope glycoprotein that lack the transmembrane anchor and cytoplasmic domains: analysis of intracellular transport and assembly into virions. J Virol. 1987; 61(10):2981-8. PMC: 255870. DOI: 10.1128/JVI.61.10.2981-2988.1987. View

Kowalski M, Potz J, Basiripour L, Dorfman T, Goh W, Terwilliger E . Functional regions of the envelope glycoprotein of human immunodeficiency virus type 1. Science. 1987; 237(4820):1351-5. DOI: 10.1126/science.3629244. View

Fukasawa M, Miura T, Hasegawa A, Morikawa S, Tsujimoto H, Miki K . Sequence of simian immunodeficiency virus from African green monkey, a new member of the HIV/SIV group. Nature. 1988; 333(6172):457-61. DOI: 10.1038/333457a0. View

10.

Vaux D, Helenius A, Mellman I . Spike--nucleocapsid interaction in Semliki Forest virus reconstructed using network antibodies. Nature. 1988; 336(6194):36-42. DOI: 10.1038/336036a0. View

11.

Owens R, Compans R . Expression of the human immunodeficiency virus envelope glycoprotein is restricted to basolateral surfaces of polarized epithelial cells. J Virol. 1989; 63(2):978-82. PMC: 247779. DOI: 10.1128/JVI.63.2.978-982.1989. View

12.

Venable R, Pastor R, Brooks B, CARSON F . Theoretically determined three-dimensional structures for amphipathic segments of the HIV-1 gp41 envelope protein. AIDS Res Hum Retroviruses. 1989; 5(1):7-22. DOI: 10.1089/aid.1989.5.7. View

13.

Whitt M, Chong L, Rose J . Glycoprotein cytoplasmic domain sequences required for rescue of a vesicular stomatitis virus glycoprotein mutant. J Virol. 1989; 63(9):3569-78. PMC: 250946. DOI: 10.1128/JVI.63.9.3569-3578.1989. View

14.

Gallaher W, Ball J, Garry R, GRIFFIN M, Montelaro R . A general model for the transmembrane proteins of HIV and other retroviruses. AIDS Res Hum Retroviruses. 1989; 5(4):431-40. DOI: 10.1089/aid.1989.5.431. View

15.

Lee S, Hu W, Fisher A, Looney D, Kao V, Mitsuya H . Role of the carboxy-terminal portion of the HIV-1 transmembrane protein in viral transmission and cytopathogenicity. AIDS Res Hum Retroviruses. 1989; 5(4):441-9. DOI: 10.1089/aid.1989.5.441. View

16.

Chakrabarti L, Emerman M, Tiollais P, Sonigo P . The cytoplasmic domain of simian immunodeficiency virus transmembrane protein modulates infectivity. J Virol. 1989; 63(10):4395-403. PMC: 251057. DOI: 10.1128/JVI.63.10.4395-4403.1989. View

17.

Kodama T, Wooley D, Naidu Y, Kestler 3rd H, Daniel M, Li Y . Significance of premature stop codons in env of simian immunodeficiency virus. J Virol. 1989; 63(11):4709-14. PMC: 251107. DOI: 10.1128/JVI.63.11.4709-4714.1989. View

18.

SCHLESINGER M . Formation of an infectious virus-antibody complex with Rous sarcoma virus and antibodies directed against the major virus glycoprotein. J Virol. 1976; 17(3):1063-7. PMC: 515508. DOI: 10.1128/JVI.17.3.1063-1067.1976. View

19.

Calafat J, Janssen H, Demant P, Hilgers J, Zavada J . Specific selection of host cell glycoproteins during assembly of murine leukaemia virus and vesicular stomatitis virus: presence of Thy-1 glycoprotein and absence of H-2, Pgp-1 and T-200 glycoproteins on the envelopes of these virus particles. J Gen Virol. 1983; 64 (Pt 6):1241-53. DOI: 10.1099/0022-1317-64-6-1241. View

20.

Russ G, Polakova K, Zavada J . Assembly of xenotropic murine leukaemia virus-related antigens from the surface of mouse L cells by vesicular stomatitis virus. Acta Virol. 1983; 27(2):105-9. View