Dimerization of the transmembrane domain of human tetherin in membrane mimetic environments

Biochemistry

Volumn 51, Issue 25, 2012, Pages 5033-5040

  Cole, Gregory ^a,b   Simonetti, Karen ^a   Ademi, Irsa ^a,b   Sharpe, Simon ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-HIV ACTIVITY; CELL SURFACE PROTEINS; COILED COIL; COILED-COIL DOMAINS; DIMERIC MOLECULES; DISULFIDE BOND FORMATION; ENVELOPED VIRUS; EXCIMER FLUORESCENCE; EXTRACELLULAR; FUNCTIONAL MODEL; HOMODIMERS; INTEGRAL MEMBRANE PROTEINS; MEMBRANE ANCHORS; MEMBRANE PROTEINS; MEMBRANE-MIMETIC ENVIRONMENTS; N-TERMINALS; SDS MICELLES; SDS-PAGE; TRANS-MEMBRANE DOMAINS; TRANSMEMBRANE REGIONS; TYPE II;

ACTIVATION ANALYSIS; CELL MEMBRANES; COVALENT BONDS; CYTOLOGY; DEGRADATION; DIMERIZATION; LIPID BILAYERS; LIPOSOMES; VIRUSES;

DISEASES;

MEMBRANE PROTEIN; TETHERIN; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; DIMERIZATION; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; LIPID BILAYER; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE;

ANTIGENS, CD; CELL MEMBRANE; GPI-LINKED PROTEINS; HIV-1; HUMANS; MEMBRANE PROTEINS; MOLECULAR MIMICRY; PEPTIDE FRAGMENTS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; TRIFLUOROETHANOL;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84862871440     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201747t     Document Type: Article

References (55)

1. Jouvenet, N., Neil, S. J. D., Zhadina, M., Zang, T., Kratovac, Z., Lee, Y., McNatt, M., Hatziioannou, T., and Bieniasz, P. D. (2009) Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin J. Virol. 83, 1837-1844
2. Neil, S. J. D., Zang, T., and Bieniasz, P. D. (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu Nature 451, 425-430 (Pubitemid 351158893)
3. Sakuma, T., Noda, T., Urata, S., Kawaoka, Y., and Yasuda, J. (2009) Inhibition of Lassa and Marberg virus production by tetherin J. Virol. 83, 2382-2385
4. 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 downregulated from the cell surface by the viral Vpu protein Cell Host Microbe 3, 245-252 (Pubitemid 351494713)
5. Perez-Caballero, D., Zang, T., Ebrahimi, A., McNatt, M. W., Gregory, D. A., Johnson, M. C., and Bienasz, P. D. (2009) Tetherin inhibits HIV-1 release by directly tethering virions to cells Cell 139, 499-511
6. Yang, H., Wang, J., Jia, X., McNatt, M. W., Zang, T., Pan, B., Meng, W., Wang, H.-W., Bienasz, 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
7. Morita, E. and Sundquist, W. (2004) Retrovirus budding Annu. Rev. Cell Dev. Biol 20, 395-425 (Pubitemid 39488644)
8. Ishikawa, J., Kaisho, T., Tomizawa, H., Lee, B. O., Kobune, Y., Inazawa, J., Oritani, K., Itoh, M., Ochi, T., Ishihara, K., and Hirano, T. (1995) Molecular cloning and chromosomal mapping pf a bone marrow stromal cell surface gene, BST2, that may be involved in pre-B-cell growth Genomics 26, 527-534
9. 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 (Pubitemid 37168591)
10. 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, xxxx
11. 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 (Pubitemid 29290312)
12. Hinz, A., Miguet, N., Natrajan, G., Usami, Y., Yamanaka, H., Renesto, P., Hartlieb, B., McCarthy, A. A., Simorre, J.-P., Gottlinger, H., and Weissenhorn, W. (2010) Structural basis of HIV-1 tethering to membranes by the Bst2/tetherin ectodomain Cell Host Microbe 7, 314-323
13. Schubert, H. L., Zhai, Q., Sandrin, V., Eckert, D. M., Garcia-Maya, M., Saul, L., Sundquist, W., Steiner, R. A., and Hill, C. P. (2010) Structural and functional studies on the extracellular domain of BST2/tetherin in reduced and oxidized conditions Proc. Natl. Acad. Sci. U. S. A. 107, 17951-17956
14. 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
15. Sakuma, T., Sakurai, A., and Yasuda, J. (2009) Dimerization of tetherin is not essential for its antiviral activity against Lassa and Marburg viruses PLoS One 4, 1-6
16. 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
17. Cohen, E. A., Terwilliger, E. F., Sodroski, J. G., and Haseltine, W. A. (1988) Identification of a Protein Encoded by the Vpu Gene of Hiv-1 Nature 334, 532-534
18. Strebel, K., Klimkait, T., Maldarelli, F., and Martin, M. A. (1989) Molecular and Biochemical Analyses of Human Immunodeficiency Virus Type-1 Vpu Protein J. Virol. 63, 3784-3791 (Pubitemid 19205450)
19. Strebel, K., Klimkait, T., and Martin, M. A. (1988) A Novel Gene of Hiv-1, Vpu, and Its 16-Kilodalton Product Science 241, 1221-1223
20. 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 (Pubitemid 20032674)
21. Terwilliger, E. F., Cohen, E. A., Lu, Y. C., Sodroski, J. G., and Haseltine, W. A. (1989) Functional-Role of Human Immunodeficiency Virus Type-1 Vpu Proc. Natl. Acad. Sci. U. S. A. 86, 5163-5167 (Pubitemid 19182254)
22. Neil, S. J. D., Eastman, S. W., Jouvenet, N., and Bieniasz, P. D. (2006) HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane PLoS Pathog. 2, 354-367 (Pubitemid 43794303)
23. 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
24. Douglas, J. L., Viswanathan, K., McCarroll, M. N., Gustin, J. K., Fruh, K., and Moses, A. V. (2009) Vpu directs the degradation of the HIV restriction factor BST-2/tetherin via a {beta}TrCP-dependent mechanism J. Virol. 83, 7931-7947
25. Goffinet, C., Allespach, I., Homann, S., Tervo, H.-M., Habermann, A., Rupp, D., Oberbremer, L., Kern, C., Tibroni, N., Welsch, S., Krijnse-Locker, J., Banting, G., Krausslich, H.-G., Fackler, O. T., and Keppler, O. T. (2009) HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor Cell Host Microbe 5, 285-297
26. Mitchell, R., Katsura, C., Skasko, M. A., Fitzpatrick, K., Lau, D., Ruiz, A., Stephens, E., Margottin-Goguet, F., Benarous, R., and Guatelli, J. C. (2009) Vpu antagonizes BST-2-mediated restriction of HIV-1 release via b-TrCP and endo-lysosomal trafficking PLoS Pathog. 5, e1000450
27. Andrew, A. and Strebel, K. (2010) HIV-1 Vpu targets cell surface markers CD4 and BST-2 through distinct mechanisms Mol. Aspects Med. 31, 407-417
28. 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. Nat. Acad. Sci. U. S. A. 106, 2868-2873
29. Gupta, R. K., Hue, 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
30. 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 human immunodeficiency virus type 1 Vpu J. Virol. 83, 7536-7546
31. Jia, B., Serra-Moreno, R., Neidermyer, W., Rahmberg, A., Mackey, J., Ben Fofana, I., 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/BST-2 PLoS Pathog. 5, 1-17
32. McNatt, M., Zhang, T., Hatziioannou, T., Bartlett, M., Ben Fofana, I., Johnson, W. E., Neil, S. J. D., and Bieniasz, P. D. (2009) Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants PLoS Pathog. 5, e1000300
33. Iwabu, Y., Fujita, H., Kinomoto, M., Kaneko, K., Ishazaka, Y., Tanaka, Y., Sata, T., and Tokunaga, K. (2009) HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin though transmembrane interactions leading to lysozomes J. Biol. Chem. 284, 35060-35072
34. Dube, M., Roy, B. B., Guiot-Guillain, P., 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
35. 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 antagonizes the innate restriction factor BST-2 via lipd-embedded helix-helix interactions J. Biol. Chem. 287, 58-67
36. Furthmayr, H. and Marchesi, V. T. (1976) Subunit structure of human erythrocyte glycophorin A Biochemistry 15, 1137-1144
37. Lemmon, M. A., Flanagan, J. M., Hunt, J. F., Adair, B. D., Bormann, B.-J., Dempsey, C. E., and Engelman, D. M. (1992) Gycophorin A dimerization is driven by specific interactions between transmembrane helices J. Biol. Chem. 267, 7683-7689
38. Melnyk, R. A., Partridge, A. W., and Deber, C. M. (2002) Transmembrane domain mediated self-assembly of major coat protein subunits from Ff bacteriophage J. Mol. Biol. 315, 63-72 (Pubitemid 34722111)
39. Melnyk, R. A., Partridge, A. W., Yip, J., Wu, Y., Goto, N. K., and Deber, C. M. (2003) Polar residue tagging of transmembrane peptides Peptide Sci. 71, 675-685 (Pubitemid 38325778)
40. Rath, A., Glibowicka, M., Nadeau, V. G., Chen, G., and Deber, C. M. (2009) Detergent binding explains anomalous SDS-PAGE migration of membrane proteins Proc. Natl. Acad. Sci. U. S. A. 106, 1760-1765
41. Lehrer, S. S. (1997) Intramolecular pyrene excimer fluorescence: a probe of proximity and protein conformational change Methods Enzymol. 278, 286-295 (Pubitemid 27229924)
42. Hammarstrom, P., Persson, M., Freskgard, P.-O., Martensson, L.-G., Andersson, D., Jonsson, B.-H., and Carlsson, U. (1999) Structural mapping of an aggregation mucleation site in a molten globule intermediate J. Biol. Chem. 274, 32897-32903 (Pubitemid 129535326)
43. Liu, W., Chen, Y., Watrob, H., Bartlett, S. G., Jen-Jacobson, L., and Barkley, M. D. (1998) N-termini of EcoRI restriction endonuclease dimer are in close proximity on the protein surface Biochemistry 37, 15457-15465 (Pubitemid 28516008)
44. TM) that is less pathogenic for pig-tailed macaques. Virology 2005, not supplied.
45. Marassi, F. M., Ma, C., Gratkowski, H., Straus, S. K., Strebel, K., Oblatt-Montal, M., Montal, M., and Opella, S. J. (1999) Correlation of the structural and functional domains in the membrane protein Vpu from HIV-1 Proc. Natl. Acad. Sci. U. S. A. 96, 14336-14341 (Pubitemid 30000651)
46. Paul, M., Mazumder, S., Raja, N., and Jabbar, M. A. (1998) Mutational analysis of the human immunodeficiency virus type 1 Vpu transmembrane domain that promotes the enhanced release of virus-like particles from the plasma membrane of mammalian cells J. Virol 72, 1270-1279 (Pubitemid 28116912)
47. Bour, S. and Strebel, K. (2003) The HIV-1 Vpu protein: a multifunctional enhancer of viral particle release Microbes Infect. 5, 1029-1039 (Pubitemid 36980856)
48. Fischer, W. B. (2003) Vpu from HIV-1 on an atomic scale: experiments and computer simulations FEBS Lett. 552, 39-46 (Pubitemid 37103007)
49. Hussain, A., Das, S. R., Ranwar, C., and Jameel, S. (2007) Oligomerization of the human immunodeficiency virus type 1 (HIV-1) Vpu protein-a genetic, biochemical and biophysical analysis Virol. J. 4, 1-11
50. Lu, J., Sharpe, S., Ghirlando, R., Yau, W.-M., and Tycko, R. (2010) Oligomerization state and supramolecular structure of the HIV-1 Vpu protein transmembrane segment in phospholipid bilayers Protein Sci. 19, 1877-1896
51. Park, S. H., Mrse, A. A., Nevzorov, A. A., Mesleh, M. F., Oblatt-Montal, M., Montal, M., and Opella, S. J. (2003) Three-dimensional structure of the channel-forming trans-membrane domain of virus protein "u" (Vpu) from HIV-1 J. Mol. Biol. 333, 409-424 (Pubitemid 37188581)
52. Schubert, U., FerrerMontiel, A. V., OblattMontal, M., Henklein, P., Strebel, K., and Montal, M. (1996) Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1-infected cells FEBS Lett. 398, 12-18 (Pubitemid 26400334)
53. Becucci, L., Cembran, A., Karim, C. B., Thomas, D. D., Guidelli, R., Gao, J., and Veglia, G. (2009) On the function of pentameric phospholamban: Ion channel or storage form? Biophys. J. 96, L60-L62
54. Cornea, R. L., Autry, J. M., Chen, Z., and Jones, L. R. (2000) Reexamination of the role of the leucine/isoleucine zipper residues of phospholamban in inhibition of the Ca2+ pump of cardiac sarcoplasmic reticulum J. Biol. Chem. 275, 41487-41494 (Pubitemid 32054985)
55. Kimura, Y., Kurzydlowski, K., Tada, M., and MacLennan, D. H. (1997) Phospholamban inhibitory function is activated by depolymerization J. Biol. Chem. 272, 15061-15064 (Pubitemid 27255517)