Basolateral sorting of the HIV type 2 and SIV envelope glycoproteins in polarized epithelial cells: Role of the cytoplasmic domain

AIDS Research and Human Retroviruses

Volumn 13, Issue 8, 1997, Pages 665-675

  Ball, Judith M ^a,b   Mulligan, Mark J ^a,c   Compans, Richard W ^d  

^a University of Alabama at Birmingham   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c University of Alabama at Birmingham   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 160; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CYTOPLASM; EPITHELIUM CELL; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINIA VIRUS; VERO CELL; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS RECOMBINANT;

EID: 0030941210     PISSN: 08892229     EISSN: None     Source Type: Journal    
DOI: 10.1089/aid.1997.13.665     Document Type: Article

References (74)

1. Compans RW and Srinivas RV: Protein sorting in polarized epithelial cells. Curr Topics Microbiol Immunol 1991;170:141-181.
2. Rodriguez-Boulan E and Nelson J: Morphogenesis of the polarized epithelial cell phenotype. Science 1989;245:718-725.
3. Simons K and van Meer G: Lipid sorting in epithelial cells. Biochemistry 1988;27:6197-6202.
4. Tucker SP and Compans RW: Virus infection of polarized epithelial cells. Adv Virus Res 1993;42:187-247.
5. Hughey PG, Compans RW, Zebedee SL, and Lamb RA: Expression of the influenza A virus M2 protein is restricted to apical surfaces of polarized epithelial cells. J Virol 1992;66:5542-5552.
6. Jones LV, Campans RW, Davis AR, Bos TJ, and Nayak DP: Surface expression of the influenza neuraminidase, an amino-terminally anchored viral membrane glycoprotein, in polarized epithelial cells. Mol Cell Biol 1985;5:2181-2189.
7. Roth MG, Compans RW, Giusti L, Davis AR, Nayak DP, Gething MJ, and Sambrook J: Influenza virus hemagglutinin expression is polarized in cells infected with recombinant SV40 viruses carrying cloned hemagglutinin DNA. Cell 1983;33:435-442.
8. Puddington L, Woodgett C, and Rose JK: Replacement of the cytoplasmic domain alters sorting of a viral glycoprotein in polarized cells. Proc Natl Acad Sci USA 1987;84:2756-2760.
9. Stephens EB, Compans RW, Earl P, and Moss B: Surface expression of viral glycoproteins in polarized epithelial cells using vaccinia virus vectors. EMBO J 1986;5:237-245.
10. Owens RJ and Compans RW: Expression of the HIV envelope glycoprotein is restricted to basolateral surfaces of polarized epithelial cells. J Virol 1989;63:978-982.
11. Owens RJ, Dubay J, Hunter E, and Compans RW: The human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells. Proc Natl Acad Sci 1991;88: 3987-3991.
12. Brewer CB and Roth MG: A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J Cell Biol 1991;114:413-421.
13. Casanova JE, Apodaca G, and Mostov KE: An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell 1991;66:65-75.
14. Hunziker W, Harter C, Matter K, and Mellman I: Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell 1991;66:907-920.
15. Matter K, Hunziker W, and Mellman I: Basolateral sorting of LDL receptor in MDCK cells: The cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell 1992;71: 741-753.
16. Prill V, Lehmann L, von Figura K, and Peters C: The cytoplasmic tail of lysosomal acid phosphatase contains overlapping but distinct signals for basolateral sorting and rapid internalization in polarized MDCK cells. EMBO J 1993;12:2181-2193.
17. Brown DA, Crise B, and Rose JK: Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 1989;245:1499-1501.
18. Lisanti MP, Le Bivic A, Sargiacomo M, and Rodriguez-Boulan E: Steady-state distribution and biogenesis of endogenous Madin-Darby canine kidney glycoproteins: Evidence for intracellular sorting and polarized cell surface delivery. J Cell Biol 1989;109:2117-2127.
19. Lisanti MP, Sargiacomo M, Graeve L, Saltiel AR, and Rodriguez-Boulan E: Polarized apical distribution of glycosol-phosphatidyl-inositol-anchored proteins in a renal epithelial cell line. Proc Natl Acad Sci USA 1988;85:9557-9561.
20. Thomas DC, Brewer CB, and Roth MG: Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine. J Biol Chem 1993;268: 3313-3320.
21. Thomas DC and Roth MG: The basolateral targeting signal in the cytoplasmic domain of glycoprotein G from vesicular stomatitis virus resembles a variety of intracellular targeting motifs related by primary sequence but having diverse targeting activities. J Biol Chem 1994;269:15732-15739.
22. Collawn JJ, Stangel M, Kuhn LA, Esekogwu V, Jing S, Trowbridge IS, and Tainer JA: Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell 1990;63:1061-1072.
23. Kristaski NT, Thomas D, and Roth MG: Characteristics of the tyrosine recognition signal for internalization of transmembrane surface glycoproteins. J Cell Biol 1990;111:1393.
24. Peters C, Braun M, Weber B, Wendland M, Schmidt B, Pohlmann R, Waheed A, and von Figura K: Targeting of a lysosomal membrane protein: A tyrosine-containing endocytosis signal in the cytoplasmic tail of lysosomal acid phosphatase is necessary and sufficient for targeting to lysosomes. EMBO J 1990;9:3497-3506.
25. Trowbridge IS: Endocytosis and signals for internalization. Curr Opin Cell Biol 1991;3:634-641.
26. Hunziker W and Mellman I: Expression of macrophage-lymphocyte Fc receptors in MDCK cells: Polarity and transcytosis differ for isoforms with or without coated pit localization domains. J Cell Biol 1989;109:3291-3302.
27. Lazarovits J and Roth M: A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits. Cell 1988;53:743-752.
28. Okamoto CT, Shia S-P, Bird C, Mostov KE, and Roth MG: The cytoplasmic domain of the polymeric immunoglobulin receptor contains two internalization signals that are distinct from its basolateral sorting signal. J Biol Chem 1992;267:9925-9932.
29. Yokode M, Pathak RK, Hammer RE, Brown MS, Goldstein JL, and Anderson RGW: Cytoplasmic sequences required for basolateral targeting of LDL receptor in livers of transgenic mice. J Cell Biol 1992;117:39-46.
30. Lodge R, Gottlinger H, Gabuzda D, Cohen EA, and Lemay G: The intracytoplasmic domain of gp41 mediates polarized budding of human immunodeficiency virus type 1 in MDCK cells. J Virol 1994;68:4857-4861.
31. Rowell JF, Stanhope PE, and Siliciano RF: Endocytosis of HIV-1 envelope protein: Mechanism and role in processing for association with class II MHC. J Immunol 1995;155:538-544.
32. Sauter MM, Pelchen-Matthews A, Bron R, Marsh M, LaBranche CC, Vance PJ, Romano J, Haggarty BS, Hart TK, Lee WMF, and Hoxie JA: An internalization signal in the simian immunodeficiency virus transmembrane protein cytoplasmic domain modulates expression of envelope glycoproteins on the cell surface. J Cell Biol 1996;132:795-811.
33. Kodama T, Wooley DP, Naidu YM, Kestler HW, Daniel MD, Li Y, and Desrosiers RC: Significance of premature stop codons in env of simian immunodeficiency virus. J Virol 1989;63:4709-4714.
34. Mulligan MJ, Yamshchikov GV, Ritter GDJ, Gao F, Jin MJ, Nail CD, Hahn BH, and Compans RW: Cytoplasmic domain truncation enhances fusion activity by the exterior glycoprotein complex of human immunodeficiency virus type 2 in selected cell types. J Virol 1992;66:3971-3975.
35. Spies CP and Compans RW: Effects of cytoplasmic domain length on cell surface expression and syncytium-forming capacity of the simian immunodeficiency virus envelope glycoprotein. Virology 1994;203:8-19.
36. Ritter GD, Mulligan MJ, Lydy SL, and Compans RW: Cell fusion activity of the simian immunodeficiency virus envelope protein is modulated by the intracytoplasmic domain. Virology 1993;197: 255-264.
37. Roth MG and Compans RW: Antibody resistant spread of vesticular stomatitis virus infection in cell lines of epithelial origin. J Virol 1980;35:547-550.
38. Sargiacomo M, Lisanti M, Graeve L, Le Bivic A, and Rodriguez-Boulan E: Integral and peripheral protein composition of the apical and basolateral membrane domains in MDCK cells. J Membr Biol 1989;107:277-286.
39. +-ATPase in polarized epithelial cells. Science 1993;260:552-554.
40. Farquhar MG and Palade GE: Junctional complexes in various epithelia. J Cell Biol 1963;17:375-412.
41. Cereijido M, Robbins ES, Dolan WJ, Rotunno CA, and Sabatini DD: Polarized monolayers formed by epithelial cells on a permeable and translucent support. J Cell Biol 1978;77:853-880.
42. Misfeldt DS, Hamamoto ST, and Pitelka DR: Transepithelial transport ion cell culture. Proc Natl Acad Sci USA 1976;73:1212-1216.
43. Steele RE, Preston AS, Johnston JP, and Handler JS: Porous-bottom dishes for culture of polarized cells. Am J Physiol 1980;251: C136-C139.
44. Lopez-Vancell R, Beaty G, Stefani E, Rodriguez-Boulan EE, and Cereijido M: Changes in paracellular and cellular ionic permeabilities of monolayers of MDCK cells with influenza or vesicular stomatitis viruses. J Membr Biol 1984;81:171-180.
45. Svensson L, Finlay BB, Bass D, von Bonsdorff CH, and Greenberg HB: Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells. J Virol 1991;65:4190-4197.
46. Albert J, Bottiger B, Biberfeld G, and Fenyö EM: Replicative and cytopathic characteristics of HIV-2 and severity of infection. Lancet 1989;1:852-853.
47. Albert J, Bredberg U, Chiodi F, Bottiger B, Fenyö EM, Njorrby E, and Biberfeld G: A new human retrovirus isolate of West African origin (SBL-6669) and its relationship to HTLV-IV, LAV-II, and HTLV-IIIB. AIDS Res Hum Retroviruses 1987;3:3-10.
48. Chakrabarti L, Emerman M, Tiollais P, and Sonigo P: The cytoplasmic domain of simian immunodeficiency virus transmembrane protein modulates infectivity. J Virol 1989;63:4395-4403.
49. Chakrabarti L, Guyader M, Alizon M, Daniel MD, Desrosiers RC, Tollais P, and Sonigo P: Sequence of simian immunodeficiency virus and its relationship to other human and simian retroviruses. Nature (London) 1987;328:543-547.
50. Evans LA, Moreau J, Odehouri K, Legg H, Barboza A, Cheng-Mayer D, and Levy JA: Characterization of a noncytopathic HIV-1 strain with unusual effects on CD4 expression. Science 1988;240:1522-1525.
51. Hasegawa A, Tsujimoto H, Maki N, Ishikawa K-I, Miura T, Fukasawa K, Miki K, and Hayami M: Genomic divergence of HIV-1 from Ghana. AIDS Res Hum Retroviruses 1989;5:593-604.
52. Kong LI, Lee S, Kappes JC, Parkin JS, Decker D, Hoxie JA, Hahn BH, and Shaw GM: West African HIV-2-related human retrovirus with attenuated cytopathicity. Science 1988;240:1525-1529.
53. Hirsch V, Riedel N, and Mullins JI: The genome organization of STLV-3 is similar to that of the AIDS virus except for a truncated transmembrane protein. Cell 1987;49:307-319.
54. Hirsch VM, Edmondson P, Murphey-Corb M, Arbeille B, Johnson PR, and Mullins JI: SFV adaption to human cells. Nature (London) 1989;341:573-574.
55. Naidum YM, Kestler HW, Li Y, Butler CV, Silva DP, Schmidt DK, Troup CD, Sehgal PK, Sonigo P, Daniel MD, and Desrosiers RC: Characterization of infectious molecular clones of simian immunodeficiency virus (SIVmac) and human immunodeficiency virus type 2: Persistent infection of rhesus monkeys with molecularly cloned SIVmac. J Virol 1988;62:4691-4696.
56. Mostov KE and Deitcher DL: Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA. Cell 1986;46:613-621.
57. Kestler H, Kodama T, Ringler D, Marthas M, Pedersen N, Lackner A, Regier D, Daniel P, King MN, and Desrosiers RC: Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 1990;248:1109-1112.
58. Spies CP, Ritter GD Jr, Mulligan MJ, and Compans RW: Truncation of the cytoplasmic domain of the dimian immunodeficiency virus envelope glycoprotein alters conformation of the external domain. J Virol 1994;68:585-591.
59. Kumar P, Hui H, Kappes JC, Haggerty BS, Hoxie JA, Arya SK, Shaw GM, and Hahn BH: Molecular characterization of an attenuated human immunodeficiency virus type 2 isolates. J Virol 1990; 64:890-901.
60. Hoxie JA, Kumar P, Hui HX, Kappes JC, and Haggarty BS: Molecular characterization of an attenuated human immunodeficiency virus type 2. J Virol 1990;64:890-901.
61. Hoxie JA, Brass LE, Pletcher CH, Haggerty BS, Colloran R, and Hahn BH: Cytopathic variants of an attenuated isolate of human immunodeficiency virus type 2 exhibit increased affinity for CD4. J Virol 1991;65:5096-5101.
62. Mulligan MJ, Kumar P, Hui H, Owens RJ, Ritter GD, Hahn BH, and Compans RW: The Env protein of an infectious noncytopathic HIV-2 is deficient in syncytium formation. AIDS Res Hum Retroviruses 1990;6:707-720.
63. Geffen I, Fuhrer C, Leitinger B, Weiss M, Huggel K, Griffiths G, and Spiess M: Related signals for endocytosis and basolateral sorting of the asialoglycoprotein receptor. J Biol Chem 1993;268: 20772-20777.
64. Williams MA and Fududa M: Accumulation of membrane glycoprotein in lysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail. J Cell Biol 1990;111:955-966.
65. Chou PY and Fasman GD: Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol 1978;47: 45-148.
66. Tashiro M, Yamakawa M, Tobita K, Klenk H-D, Rott R, and Seto JT: Organ tropism of Sendai virus in mice: Proteolytic activation of the fusion glycoprotein in mouse organs and budding sites at the bronchial epithelium. J Virol 1990;64:3627-3634.
67. Fantini J, Yahi N, Baghdiguian S, and Chermann J-C: Human colon epithelial cells productively infected with human immunodeficiency virus show impaired differentiation and altered secretion. J Virol 1992;66:580-585.
68. Mathjis JM, Hing MC, Grierson J, Dwyer DE, Goldschmidt C, Cooper DA, and Cunningham AL: HIV infection of rectal mucosa. Lancet 1988;i:1111.
69. Moyer MP, Hout RI, Ramirez A, Joe S, Meltzer MS, and Gendelman HE: Infection of human gastrointestinal cells by HIV-1. AIDS Res Hum Retroviruses 1990;6:1409-1415.
70. Nelson JA, Renolds-Kohler C, Margaretten W, Wiley CA, Reese CE, and Levy JA: Human immunodeficiency virus detected in bowel epithelium from patients with gastrointestinal symptoms. Lancet 1988;i:259-262.
71. Groopman JE, Salahuddin SZ, Sarngadharan MG, Markham PD, Gonda M, Sliski A, and Gallo RC: HTLV-III in saliva of people with AIDS-related complex and healthy homosexual men at risk for AIDS. Science 1984;226:447-449.
72. Ho SN, Hunt HD, Horton RM, Pullen JK, and Pease LR: Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989;77:51-59.
73. Zagury D, Bernard J, Leibowitch J, Safai B, Groopman JE, Feldman M, Sarngadharan MF, and Gallo RC: HTLV-III in cells cultured from semen of two patients with AIDS. Science 1984;226: 449-451.
74. Miller CJ, Alexander NJ, Sutjipto S, Lackner AA, Hendrickx AG, Gettie A, Lowenstine LJ, Jennings M, and Marx PA: Genital mucosal transmission of simian immunodeficiency virus: Animal model for heterosexual transmission of human immunodeficiency virus. J Virol 1989;63:4277-4284.