Virion stiffness regulates immature HIV-1 entry

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Pang, Hong Bo ^a,c   Hevroni, Liron ^b   Kol, Nitzan ^b   Eckert, Debra M ^a   Tsvitov, Marianna ^b   Kay, Michael S ^a   Rousso, Itay ^b,d  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c BURNHAM INSTITUTE   (United States)

^d BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Atomic force microscopy; HIV; Maturation; Stiffness; Viral entry

Indexed keywords

VIRUS ENVELOPE PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PROTEIN DOMAIN; VESICULAR STOMATITIS VIRUS; VIRION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS PARTICLE; VIRUS REPLICATION;

ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HUMANS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; VIRAL MATRIX PROTEINS; VIRION; VIRUS INTERNALIZATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84872107953     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-4     Document Type: Article

References (41)

1. Wills JW, Craven RC. Form, function, and use of retroviral gag proteins. AIDS 1991, 5:639-654. 10.1097/00002030-199106000-00002, 1883539.
2. Berger EA, Murphy PM, Farber JM. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 1999, 17:657-700. 10.1146/annurev.immunol.17.1.657, 10358771.
3. Chan DC, Kim PS. HIV entry and its inhibition. Cell 1998, 93:681-684. 10.1016/S0092-8674(00)81430-0, 9630213.
4. Wyma DJ, Kotov A, Aiken C. Evidence for a stable interaction of gp41 with Pr55(Gag) in immature human immunodeficiency virus type 1 particles. J Virol 2000, 74:9381-9387. 10.1128/JVI.74.20.9381-9387.2000, 112366, 11000206.
5. Cosson P. Direct interaction between the envelope and matrix proteins of HIV-1. EMBO J 1996, 15:5783-5788. 452325, 8918455.
6. Jiang J, Aiken C. Maturation-dependent human immunodeficiency virus type 1 particle fusion requires a carboxyl-terminal region of the gp41 cytoplasmic tail. J Virol 2007, 81:9999-10008. 10.1128/JVI.00592-07, 2045384, 17609279.
7. Swanstrom R, Wills JW. Synthesis, assembly, and processing of viral proteins in retrovirus 1997, 263-334. Plainview, NY: Cold Spring Harbor Laboratory Press.
8. Coffin JM, Hughes SH, Varmus HE. Retroviruses 1997, Plainview, NY: Cold Spring Harbor Laboratory Press.
9. Kol N, Gladnikoff M, Barlam D, Shneck RZ, Rein A, Rousso I. Mechanical properties of murine leukemia virus particles: effect of maturation. Biophys J 2006, 91:767-774. 10.1529/biophysj.105.079657, 1483117, 16632508.
10. Ivanovska IL, de Pablo PJ, Ibarra B, Sgalari G, MacKintosh FC, Carrascosa JL, Schmidt CF, Wuite GJ. Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc Natl Acad Sci U S A 2004, 101:7600-7605. 10.1073/pnas.0308198101, 419652, 15133147.
11. Michel JP, Ivanovska IL, Gibbons MM, Klug WS, Knobler CM, Wuite GJ, Schmidt CF. Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proc Natl Acad Sci U S A 2006, 103:6184-6189. 10.1073/pnas.0601744103, 1458852, 16606825.
12. Carrasco C, Carreira A, Schaap IA, Serena PA, Gomez-Herrero J, Mateu MG, de Pablo PJ. DNA-mediated anisotropic mechanical reinforcement of a virus. Proc Natl Acad Sci U S A 2006, 103:13706-13711. 10.1073/pnas.0601881103, 1564217, 16945903.
13. Kol N, Shi Y, Tsvitov M, Barlam D, Shneck RZ, Kay MS, Rousso I. A stiffness switch in human immunodeficiency virus. Biophys J 2007, 92:1777-1783. 10.1529/biophysj.106.093914, 1796819, 17158573.
14. Wyma DJ, Jiang J, Shi J, Zhou J, Lineberger JE, Miller MD, Aiken C. Coupling of human immunodeficiency virus type 1 fusion to virion maturation: a novel role of the gp41 cytoplasmic tail. J Virol 2004, 78:3429-3435. 10.1128/JVI.78.7.3429-3435.2004, 371074, 15016865.
15. Murakami T, Ablan S, Freed EO, Tanaka Y. Regulation of human immunodeficiency virus type 1 Env-mediated membrane fusion by viral protease activity. J Virol 2004, 78:1026-1031. 10.1128/JVI.78.2.1026-1031.2004, 368813, 14694135.
16. Edwards TG, Wyss S, Reeves JD, Zolla-Pazner S, Hoxie JA, Doms RW, Baribaud F. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein. J Virol 2002, 76:2683. 10.1128/JVI.76.6.2683-2691.2002, 135967, 11861835.
17. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 2009, 137:433-444. 10.1016/j.cell.2009.02.046, 2696170, 19410541.
18. Superti F, Seganti L, Ruggeri FM, Tinari A, Donelli G, Orsi N. Entry pathway of vesicular stomatitis virus into different host cells. J Gen Virol 1987, 68(Pt 2):387-399.
19. Marsh M, Helenius A. Virus entry: open sesame. Cell 2006, 124:729-740. 10.1016/j.cell.2006.02.007, 16497584.
20. Sader JE, Chon JW, Mulvaney P. Calibration of rectangular atomic force microscope cantilevers. Rev Sci Instrum 1999, 70:3967-3969.
21. Dong XN, Xiao Y, Dierich MP, Chen YH. N- and C-domains of HIV-1 gp41: mutation, structure and functions. Immunol Lett 2001, 75:215-220. 10.1016/S0165-2478(00)00302-3, 11166378.
22. Chen BK, Gandhi RT, Baltimore D. CD4 down-modulation during infection of human T cells with human immunodeficiency virus type 1 involves independent activities of vpu, env, and nef. J Virol 1996, 70:6044-6053. 190625, 8709227.
23. Wu Z, Alexandratos J, Ericksen B, Lubkowski J, Gallo RC, Lu W. Total chemical synthesis of N-myristoylated HIV-1 matrix protein p17: structural and mechanistic implications of p17 myristoylation. Proc Natl Acad Sci U S A 2004, 101:11587-11592. 10.1073/pnas.0404649101, 511025, 15280532.
24. Ganser-Pornillos BK, Yeager M, Sundquist WI. The structural biology of HIV assembly. Curr Opin Struct Biol 2008, 18:203-217. 10.1016/j.sbi.2008.02.001, 2819415, 18406133.
25. Zhu P, Liu J, Bess J, Chertova E, Lifson JD, Grise H, Ofek GA, Taylor KA, Roux KH. Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 2006, 441:847-852. 10.1038/nature04817, 16728975.
26. Cimarelli A, Darlix JL. Assembling the human immunodeficiency virus type 1. Cell Mol Life Sci 2002, 59:1166-1184. 10.1007/s00018-002-8495-6, 12222963.
27. Frankel AD, Young JA. HIV-1: fifteen proteins and an RNA. Annu Rev Biochem 1998, 67:1-25. 10.1146/annurev.biochem.67.1.1, 9759480.
28. Turner BG, Summers MF. Structural biology of HIV. J Mol Biol 1999, 285:1-32. 10.1006/jmbi.1998.2354, 9878383.
29. Waheed AA, Ablan SD, Mankowski MK, Cummins JE, Ptak RG, Schaffner CP, Freed EO. Inhibition of HIV-1 replication by amphotericin B methyl ester: selection for resistant variants. J Biol Chem 2006, 281:28699-28711. 10.1074/jbc.M603609200, 16882663.
30. Waheed AA, Ablan SD, Roser JD, Sowder RC, Schaffner CP, Chertova E, Freed EO. HIV-1 escape from the entry-inhibiting effects of a cholesterol-binding compound via cleavage of gp41 by the viral protease. Proc Natl Acad Sci U S A 2007, 104:8467-8471. 10.1073/pnas.0701443104, 1895973, 17483482.
31. Brugger B, Glass B, Haberkant P, Leibrecht I, Wieland FT, Krausslich HG. The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci U S A 2006, 103:2641-2646. 10.1073/pnas.0511136103, 1413831, 16481622.
32. Aloia RC, Tian H, Jensen FC. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc Natl Acad Sci U S A 1993, 90:5181-5185. 10.1073/pnas.90.11.5181, 46679, 8389472.
33. Dehart JL, Andersen JL, Zimmerman ES, Ardon O, An DS, Blackett J, Kim B, Planelles V. The ataxia telangiectasia-mutated and Rad3-related protein is dispensable for retroviral integration. J Virol 2005, 79:1389-1396. 10.1128/JVI.79.3.1389-1396.2005, 544104, 15650165.
34. Chen BK, Saksela K, Andino R, Baltimore D. Distinct modes of human immunodeficiency virus type 1 proviral latency revealed by superinfection of nonproductively infected cell lines with recombinant luciferase-encoding viruses. J Virol 1994, 68:654-660. 236499, 7507183.
35. Yee JK, Miyanohara A, LaPorte P, Bouic K, Burns JC, Friedmann T. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc Natl Acad Sci U S A 1994, 91:9564-9568. 10.1073/pnas.91.20.9564, 44853, 7937806.
36. O'Rourke JP, Olsen JC, Bunnell BA. Optimization of equine infectious anemia derived vectors for hematopoietic cell lineage gene transfer. Gene Ther 2005, 12:22-29. 10.1038/sj.gt.3302350, 15550928.
37. Binley JM, Cayanan CS, Wiley C, Schulke N, Olson WC, Burton DR. Redox-triggered infection by disulfide-shackled human immunodeficiency virus type 1 pseudovirions. J Virol 2003, 77:5678-5684. 10.1128/JVI.77.10.5678-5684.2003, 154040, 12719560.
38. Dubay JW, Roberts SJ, Hahn BH, Hunter E. Truncation of the human immunodeficiency virus type 1 transmembrane glycoprotein cytoplasmic domain blocks virus infectivity. J Virol 1992, 66:6616-6625. 240157, 1357190.
39. Hamburger AE, Kim S, Welch BD, Kay MS. Steric accessibility of the HIV-1 gp41 N-trimer region. J Biol Chem 2005, 280:12567-12572.
40. Kol N, Tsvitov M, Hevroni L, Wolf SG, Pang HB, Kay MS, Rousso I. The effect of purification method on the completeness of the immature HIV-1 Gag shell. J Virol Methods 2010, 169:244-247. 10.1016/j.jviromet.2010.07.035, 20691213.
41. Hutter JL, Bechhoefer J. Calibration of atomic-force microscopy tips. Rev Sci Instrum 1993, 64:1868-1873.