The size and conservation of a coiled-coil structure in the ectodomain of human BST-2/tetherin is dispensable for inhibition of HIV-1 virion release

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44278-44288

  Andrew, Amy J ^a   Berndsen, Christopher E ^b   Kao, Sandra ^a   Strebel, Klaus ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b JAMES MADISON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COILED COIL; COILED-COIL DOMAINS; COILED-COIL STRUCTURE; DIMER INTERFACE; ECTODOMAIN; FUNCTIONAL PROPERTIES; HYDROPHOBIC RESIDUES; STRUCTURAL STUDIES;

BIOCHEMISTRY; BIOLOGY;

DISEASES;

BST 2 PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; VIRION; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS RELEASE;

AMINO ACID SEQUENCE; ANTIGENS, CD; DIMERIZATION; DOWN-REGULATION; GPI-LINKED PROTEINS; HELA CELLS; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; VIRION; VIRUS RELEASE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84871761298     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.418822     Document Type: Article

References (59)

1. Van Damme, N., Goff, D., Katsura, C., Jorgenson, R. L., Mitchell, R., Johnson, M. C., Stephens, E. B., and Guatelli, J. (2008) The interferon-induced protein BST-2 restricts HIV-1 release and is down-regulated from the cell surface by the viral Vpu protein. Cell. Host. Microbe. 3, 245-252
2. Neil, S. J., Zang, T., and Bieniasz, P. D. (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430
3. Gupta, R. K., Hué, S., Schaller, T., Verschoor, E., Pillay, D., and Towers, G. J. (2009) Mutation of a single residue renders human tetherin resistant to HIV-1 Vpu-mediated depletion. PLoS Pathog. 5, e1000443
4. Jia, B., Serra-Moreno, R., Neidermyer, W., Rahmberg, A., Mackey, J., Fofana, I. B., Johnson, W. E., Westmoreland, S., and Evans, D. T. (2009) Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 5, e1000429
5. Hauser, H., Lopez, L. A., Yang, S. J., Oldenburg, J. E., Exline, C. M., Guatelli, J. C., and Cannon, P. M. (2010) HIV-1 Vpu and HIV-2 Env counteract BST-2/tetherin by sequestration in a perinuclear compartment. Retrovirology 7, 51
6. Le Tortorec, A., and Neil, S. J. (2009) Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J. Virol. 83, 11966-11978
7. Sauter, D., Schindler, M., Specht, A., Landford, W. N., Münch, J., Kim, K. A., Votteler, J., Schubert, U., Bibollet-Ruche, F., Keele, B. F., Takehisa, J., Ogando, Y., Ochsenbauer, C., Kappes, J. C., Ayouba, A., Peeters, M., Learn, G. H., Shaw, G., Sharp, P. M., Bieniasz, P., Hahn, B. H., Hatziioannou, T., and Kirchhoff, F. (2009) Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6, 409-421
8. Yang, S. J., Lopez, L. A., Hauser, H., Exline, C. M., Haworth, K. G., and Cannon, P. M. (2010) Anti-tetherin activities in Vpu-expressing primate lentiviruses. Retrovirology 7, 13
9. Zhang, F., Wilson, S. J., Landford, W. C., Virgen, B., Gregory, D., Johnson, M. C., Munch, J., Kirchhoff, F., Bieniasz, P. D., and Hatziioannou, T. (2009) Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6, 54-67
10. Kobayashi, T., Ode, H., Yoshida, T., Sato, K., Gee, P., Yamamoto, S. P., Ebina, H., Strebel, K., Sato, H., and Koyanagi, Y. (2011) Identification of amino acids in the human tetherin transmembrane domain responsible for HIV-1 Vpu interaction and susceptibility. J. Virol. 85, 932-945
11. Yoshida, T., Kao, S., and Strebel, K. (2011) Identification of residues in the BST-2 TM domain important for antagonism by HIV-1 Vpu using a gain-of-function approach. Front. Microbiol. 2, 35
12. Rong, L., Zhang, J., Lu, J., Pan, Q., Lorgeoux, R. P., Aloysius, C., Guo, F., Liu, S. L., Wainberg, M. A., and Liang, C. (2009) The transmembrane domain of BST-2 determines its sensitivity to down-modulation by HIV-1 Vpu. J. Virol. 83, 7536-7546
13. Mangeat, B., Gers-Huber, G., Lehmann, M., Zufferey, M., Luban, J., and Piguet, V. (2009) HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog. 5, e1000574
14. Dubé, M., Roy, B. B., Guiot-Guillain, P., Binette, J., Mercier, J., Chiasson, A., and Cohen, E. A. (2010) Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathog. 6, e1000856
15. Douglas, J. L., Viswanathan, K., McCarroll, M. N., Gustin, J. K., Früh, K., and Moses, A. V. (2009) Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a βTrCP-dependent mechanism. J. Virol. 83, 7931-7947
16. Vigan, R., and Neil, S. J. (2011) Separable determinants of subcellular localization and interaction account for the inability of group O HIV-1 Vpu to counteract tetherin. J. Virol. 85, 9737-9748
17. Skasko, M., Wang, Y., Tian, Y., Tokarev, A., Munguia, J., Ruiz, A., Stephens, E. B., Opella, S. J., and Guatelli, J. (2012) HIV-1 Vpu protein antagonizes innate restriction factor BST-2 via lipid-embedded helix-helix interactions. J. Biol. Chem. 287, 58-67
18. Zhou, J., Zhang, Z., Mi, Z., Wang, X., Zhang, Q., Li, X., Liang, C., and Cen, S. (2012) Characterization of the interface of the bone marrow stromal cell antigen 2-Vpu protein complex via computational chemistry. Biochemistry 51, 1288-1296
19. Kueck, T., and Neil, S. J. (2012) A cytoplasmic tail determinant in HIV-1 Vpu mediates targeting of tetherin for endosomal degradation and counteracts interferon-induced restriction. PLoS Pathog. 8, e1002609
20. Ohtomo, T., Sugamata, Y., Ozaki, Y., Ono, K., Yoshimura, Y., Kawai, S., Koishihara, Y., Ozaki, S., Kosaka, M., Hirano, T., and Tsuchiya, M. (1999) Molecular cloning and characterization of a surface antigen preferentially overexpressed on multiple myeloma cells. Biochem. Biophys. Res. Commun. 258, 583-591
21. Goto, T., Kennel, S. J., Abe, M., Takishita, M., Kosaka, M., Solomon, A., and Saito, S. (1994) A novel membrane antigen selectively expressed on terminally differentiated human B cells. Blood 84, 1922-1930
22. Ishikawa, J., Kaisho, T., Tomizawa, H., Lee, B. O., Kobune, Y., Inazawa, J., Oritani, K., Itoh, M., Ochi, T., and Ishihara, K. (1995) Molecular cloning and chromosomal mapping of a bone marrow stromal cell surface gene, BST2, that may be involved in pre-B-cell growth. Genomics 26, 527-534
23. Kupzig, S., Korolchuk, V., Rollason, R., Sugden, A., Wilde, A., and Banting, G. (2003) Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 4, 694-709
24. Andrew, A. J., Kao, S., and Strebel, K. (2011) C-terminal hydrophobic region in human bone marrow stromal cell antigen 2 (BST-2)/tetherin protein functions as second transmembrane motif. J. Biol. Chem. 286, 39967-39981
25. Hinz, A., Miguet, N., Natrajan, G., Usami, Y., Yamanaka, H., Renesto, P., Hartlieb, B., McCarthy, A. A., Simorre, J. P., Göttlinger, H., and Weissenhorn, W. (2010) Structural basis of HIV-1 tethering to membranes by the BST-2/tetherin ectodomain. Cell Host Microbe 7, 314-323
26. Schubert, H. L., Zhai, Q., Sandrin, V., Eckert, D. M., Garcia-Maya, M., Saul, L., Sundquist, W. I., Steiner, R. A., and Hill, C. P. (2010) Structural and functional studies on the extracellular domain of BST2/tetherin in reduced and oxidized conformations. Proc. Natl. Acad. Sci. U.S.A. 107, 17951-17956
27. Yang, H., Wang, J., Jia, X., McNatt, M. W., Zang, T., Pan, B., Meng, W., Wang, H. W., Bieniasz, P. D., and Xiong, Y. (2010) Structural insight into the mechanisms of enveloped virus tethering by tetherin. Proc. Natl. Acad. Sci. U.S.A. 107, 18428-18432
28. Swiecki, M., Scheaffer, S. M., Allaire, M., Fremont, D. H., Colonna, M., and Brett, T. J. (2011) Structural and biophysical analysis of BST-2/tetherin ectodomains reveals an evolutionary conserved design to inhibit virus release. J. Biol. Chem. 286, 2987-2997
29. Andrew, A. J., Miyagi, E., Kao, S., and Strebel, K. (2009) The formation of cysteine-linked dimers of BST-2/tetherin is important for inhibition of HIV-1 virus release but not for sensitivity to Vpu. Retrovirology 6, 80
30. Perez-Caballero, D., Zang, T., Ebrahimi, A., McNatt, M. W., Gregory, D. A., Johnson, M. C., and Bieniasz, P. D. (2009) Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139, 499-511
31. Masuyama, N., Kuronita, T., Tanaka, R., Muto, T., Hirota, Y., Takigawa, A., Fujita, H., Aso, Y., Amano, J., and Tanaka, Y. (2009) HM1.24 is internalized from lipid rafts by clathrin-mediated endocytosis through interaction with α-adaptin. J. Biol. Chem. 284, 15927-15941
32. Rollason, R., Korolchuk, V., Hamilton, C., Schu, P., and Banting, G. (2007) Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. J. Cell. Sci. 120, 3850-3858
33. Fritz, J. V., Tibroni, N., Keppler, O. T., and Fackler, O. T. (2012) HIV-1 Vpu's lipid raft association is dispensable for counteraction of the particle release restriction imposed by CD317/tetherin. Virology 424, 33-44
34. Lopez, L. A., Yang, S. J., Exline, C. M., Rengarajan, S., Haworth, K. G., and Cannon, P. M. (2012) Anti-tetherin activities of HIV-1 Vpu and Ebola virus glycoprotein do not involve removal of tetherin from lipid rafts. J. Virol. 86, 5467-5480
35. Fitzpatrick, K., Skasko, M., Deerinck, T. J., Crum, J., Ellisman, M. H., and Guatelli, J. (2010) Direct restriction of virus release and incorporation of the interferon-induced protein BST-2 into HIV-1 particles. PLoS Pathog. 6, e1000701
36. Habermann, A., Krijnse-Locker, J., Oberwinkler, H., Eckhardt, M., Homann, S., Andrew, A., Strebel, K., and Kräusslich, H. G. (2010) CD317/tetherin is enriched in the HIV-1 envelope and down-regulated from the plasma membrane upon virus infection. J. Virol. 84, 4646-4658
37. Hammonds, J., Wang, J. J., Yi, H., and Spearman, P. (2010) Immunoelectron microscopic evidence for tetherin/BST2 as the physical bridge between HIV-1 virions and the plasma membrane. PLoS Pathog. 6, e1000749
38. Jones, P. H., Mehta, H. V., Maric, M., Roller, R. J., and Okeoma, C. M. (2012) Bone marrow stromal cell antigen 2 (BST-2) restricts mouse mammary tumor virus (MMTV) replication in vivo. Retrovirology 9, 10
39. Hammonds, J., Ding, L., Chu, H., Geller, K., Robbins, A., Wang, J. J., Yi, H., and Spearman, P. (2012) The tetherin/BST-2 coiled-coil ectodomain mediates plasma membrane microdomain localization and restriction of particle release. J. Virol. 86, 2259-2272
40. Adachi, A., Gendelman, H. E., Koenig, S., Folks, T., Willey, R., Rabson, A., and Martin, M. A. (1986) Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59, 284-291
41. Klimkait, T., Strebel, K., Hoggan, M. D., Martin, M. A., and Orenstein, J. M. (1990) The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J. Virol. 64, 621-629
42. Lupas, A., Van Dyke, M., and Stock, J. (1991) Predicting coiled coils from protein sequences. Science 252, 1162-1164
43. Miyagi, E., Andrew, A. J., Kao, S., and Strebel, K. (2009) Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface down-modulation and intracellular depletion. Proc. Natl. Acad. Sci. U.S.A. 106, 2868-2873
44. Van Durme, J., Delgado, J., Stricher, F., Serrano, L., Schymkowitz, J., and Rousseau, F. (2011) A graphical interface for the FoldX forcefield. Bioinformatics 27, 1711-1712
45. Krieger, E., Koraimann, G., and Vriend, G. (2002) Increasing the precision of comparative models with YASARA NOVA. A self-parameterizing force field. Proteins 47, 393-402
46. Delorenzi, M., and Speed, T. (2002) An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18, 617-625
47. Bartoli, L., Fariselli, P., Krogh, A., and Casadio, R. (2009) CCHMM-PROF. A HMM-based coiled-coil predictor with evolutionary information. Bioinformatics 25, 2757-2763
48. Berger, B., Wilson, D. B., Wolf, E., Tonchev, T., Milla, M., and Kim, P. S. (1995) Predicting coiled coils by use of pairwise residue correlations. Proc. Natl. Acad. Sci. U.S.A. 92, 8259-8263
49. McDonnell, A. V., Jiang, T., Keating, A. E., and Berger, B. (2006) Paircoil2. Improved prediction of coiled-coils from sequence. Bioinformatics 22, 356-358
50. Fischetti, V. A., Landau, G. M., Sellers, P. H., and Schmidt, J. P. (1993) Identifying periodic occurences of a template with applications to protein structure. Inf. Process. Lett. 45, 11-18
51. Cole, C., Barber, J. D., and Barton, G. J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201
52. Andrew, A., and Strebel, K. (2011) The interferon-inducible host factor bone marrow stromal antigen 2/tetherin restricts virion release, but is it actually a viral restriction factor? J. Interferon. Cytokine Res. 31, 137-144
53. Crick, F. H. (1953) The packing of α-helices. Simple coiled-coils. Acta Crystallogr. 6, 689-697
54. + cells. J. Virol. 85, 11981-11994
55. Wagschal, K., Tripet, B., Lavigne, P., Mant, C., and Hodges, R. S. (1999) The role of position a in determining the stability and oligomerization state of α-helical coiled coils. 20 amino acid stability coefficients in the hydrophobic core of proteins. Protein Sci. 8, 2312-2329
56. Tripet, B., Wagschal, K., Lavigne, P., Mant, C. T., and Hodges, R. S. (2000) Effects of side-chain characteristics on stability and oligomerization state of a de novo-designed model coiled-coil. 20 amino acid substitutions in position "d." J. Mol. Biol. 300, 377-402
57. Pace, C. N., and Scholtz, J. M. (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys. J. 75, 422-427
58. Lu, S. M., and Hodges, R. S. (2004) Defining the minimum size of a hydrophobic cluster in two-stranded α-helical coiled-coils. Effects on protein stability. Protein Sci. 13, 714-726
59. Kwok, S. C., and Hodges, R. S. (2004) Effect of chain length on coiled-coil stability. Decreasing stability with increasing chain length. Biopolymers 76, 378-390