A two-pronged structural analysis of retroviral maturation indicates that core formation proceeds by a disassembly-reassembly pathway rather than a displacive transition

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13655-13664

  Keller, Paul W ^a   Huang, Rick K ^a   England, Matthew R ^b   Waki, Kayoko ^c   Cheng, Naiqian ^a   Bernard Heymann, J ^a   Craven, Rebecca C ^b   Freed, Eric O ^c   Steven, Alasdair C ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; GAG PROTEIN; SPACER PEPTIDE; SPACER PEPTIDE 1; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; RETROVIRUS; ROUS SARCOMA ONCOVIRUS; STRUCTURE ANALYSIS; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS INFECTIVITY; VIRUS PARTICLE;

CAPSID; CAPSID PROTEINS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENE PRODUCTS, GAG; HIV-1; HUMANS; MODELS, MOLECULAR; MUTATION; ROUS SARCOMA VIRUS;

EID: 84888036006     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01408-13     Document Type: Article

References (58)

1. Wlodawer A, Vondrasek J. 1998. Inhibitors of HIV-1 protease:a major success of structure-assisted drug design. Annu. Rev. Biophys. Biomol. Struct. 27:249-284.
2. Adamson CS, Salzwedel K, Freed EO. 2009. Virus maturation as a new HIV-1 therapeutic target. Expert Opin. Ther. Targets 13:895-908.
3. Zhou J, Huang L, Hachey DL, Chen CH, Aiken C. 2005. Inhibition of HIV-1 maturation via drug association with the viral Gag protein in immature HIV-1 particles. J. Biol. Chem. 280:42149-42155.
4. Ganser-Pornillos BK, Yeager M, Sundquist WI. 2008. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18:203-217.
5. Freed EO. 1998. HIV-1 gag proteins:diverse functions in the virus life cycle. Virology 251:1-15.
6. Heymann JB, Butan C, Winkler DC, Craven RC, Steven AC. 2008. Irregular and semi-regular polyhedral models for Rous sarcoma virus cores. Comput. Math. Methods Med. 9:197-210.
7. Ganser-Pornillos BK, von Schwedler UK, Stray KM, Aiken C, Sundquist WI. 2004. Assembly properties of the human immunodeficiency virus type 1 CA protein. J. Virol. 78:2545-2552.
8. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283:80-83.
9. Pornillos O, Ganser-Pornillos BK, Yeager M. 2011. Atomic-level modelling of the HIV capsid. Nature 469:424-427.
10. Cardone G, Purdy JG, Cheng N, Craven RC, Steven AC. 2009. Visualization of a missing link in retrovirus capsid assembly. Nature 457:694-698.
11. Li S, Hill CP, Sundquist WI, Finch JT. 2000. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407:409-413.
12. Briggs JA, Riches JD, Glass B, Bartonova V, Zanetti G, Kräusslich HG. 2009. Structure and assembly of immature HIV. Proc. Natl. Acad. Sci. U.S.A. 106:11090-11095.
13. Wright ER, Schooler JB, Ding HJ, Kieffer C, Fillmore C, Sundquist WI, Jensen GJ. 2007. Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J. 26:2218-2226.
14. Ganser-Pornillos BK, Cheng A, Yeager M. 2007. Structure of full-length HIV-1 CA:a model for the mature capsid lattice. Cell 131:70-79.
15. Campos-Olivas R, Newman JL, Summers MF. 2000. Solution structure and dynamics of the Rous sarcoma virus capsid protein and comparison with capsid proteins of other retroviruses. J. Mol. Biol. 296:633-649.
16. Pornillos O, Ganser-Pornillos BK, Kelly BN, Hua Y, Whitby FG, Stout CD, Sundquist WI, Hill CP, Yeager M. 2009. X-ray structures of the hexameric building block of the HIV capsid. Cell 137:1282-1292.
17. Mortuza GB, Haire LF, Stevens A, Smerdon SJ, Stoye JP, Taylor IA. 2004. High-resolution structure of a retroviral capsid hexameric aminoterminal domain. Nature 431:481-485.
18. Kingston RL, Fitzon-Ostendorp T, Eisenmesser EZ, Schatz GW, Vogt VM, Post CB, Rossmann MG. 2000. Structure and self-association of the Rous sarcoma virus capsid protein. Structure 8:617-628.
19. Macek P, Chmelik J, Krizova I, Kaderavek P, Padrta P, Zidek L, Wildova M, Hadravova R, Chaloupkova R, Pichova I, Ruml T, Rumlova M, Sklenar V. 2009. NMR structure of the N-terminal domain of capsid protein from the Mason-Pfizer monkey virus. J. Mol. Biol. 392:100-114.
20. Lanman J, Lam TT, Barnes S, Sakalian M, Emmett MR, Marshall AG, Prevelige PE, Jr. 2003. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J. Mol. Biol. 325:759-772.
21. Monroe EB, Kang S, Kyere SK, Li R, Prevelige PE, Jr. 2010. Hydrogen/ deuterium exchange analysis of HIV-1 capsid assembly and maturation. Structure 18:1483-1491.
22. Byeon IJ, Meng X, Jung J, Zhao G, Yang R, Ahn J, Shi J, Concel J, Aiken C, Zhang P, Gronenborn AM. 2009. Structural convergence between cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function. Cell 139:780-790.
23. Meng X, Zhao G, Yufenyuy E, Ke D, Ning J, Delucia M, Ahn J, Gronenborn AM, Aiken C, Zhang P. 2012. Protease cleavage leads to formation of mature trimer interface in HIV-1 capsid. PLoS Pathog. 8:e1002886. doi:10.1371/journal.ppat.1002886.
24. Bharat TA, Davey NE, Ulbrich P, Riches JD, de Marco A, Rumlova M, Sachse C, Ruml T, Briggs JA. 2012. Structure of the immature retroviral capsid at 8 Å resolution by cryo-electron microscopy. Nature 487:385-389.
25. Swanstrom R, Wills JW. 1997. Synthesis, assembly, and processing of viral proteins, p 263-334. In Coffin JM, Hughes SH, Varmus H (ed), Retroviruses. Cold Spring Harbor Laboratory Press, Woodbury, NY.
26. Wiegers K, Rutter G, Kottler H, Tessmer U, Hohenberg H, Krausslich HG. 1998. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J. Virol. 72:2846-2854.
27. Pettit SC, Moody MD, Wehbie RS, Kaplan AH, Nantermet PV, Klein CA, Swanstrom R. 1994. The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J. Virol. 68:8017-8027.
28. Lee SK, Potempa M, Kolli M, Ozen A, Schiffer CA, Swanstrom R. 2012. Context surrounding processing sites is crucial in determining cleavage rate of a subset of processing sites in HIV-1 Gag and Gag-Pro-Pol polyprotein precursors by viral protease. J. Biol. Chem. 287:13279-13290.
29. de Marco A, Muller B, Glass B, Riches JD, Kräusslich HG, Briggs JA. 2010. Structural analysis of HIV-1 maturation using cryo-electron tomography. PLoS Pathog. 6:e1001215. doi:10.1371/journal.ppat.1001215.
30. Adamson CS, Freed EO. 2007. Human immunodeficiency virus type 1 assembly, release, and maturation. Adv. Pharmacol. 55:347-387.
31. Datta SA, Temeselew LG, Crist RM, Soheilian F, Kamata A, Mirro J, Harvin D, Nagashima K, Cachau RE, Rein A. 2011. On the role of the SP1 domain in HIV-1 particle assembly:a molecular switch? J. Virol. 85:4111-4121.
32. Accola MA, Hoglund S, Göttlinger HG. 1998. A putative alpha-helical structure which overlaps the capsid-p2 boundary in the human immunodeficiency virus type 1 Gag precursor is crucial for viral particle assembly. J. Virol. 72:2072-2078.
33. Keller PW, Johnson MC, Vogt VM. 2008. Mutations in the spacer peptide and adjoining sequences in Rous sarcoma virus Gag lead to tubular budding. J. Virol. 82:6788-6797.
34. Krausslich HG, Facke M, Heuser AM, Konvalinka J, Zentgraf H. 1995. The spacer peptide between human immunodeficiency virus capsid and nucleocapsid proteins is essential for ordered assembly and viral infectivity. J. Virol. 69:3407-3419.
35. Li F, Goila-Gaur R, Salzwedel K, Kilgore NR, Reddick M, Matallana C, Castillo A, Zoumplis D, Martin DE, Orenstein JM, Allaway GP, Freed EO, Wild CT. 2003. PA-457:a potent HIV inhibitor that disrupts core condensation by targeting a late step in Gag processing. Proc. Natl. Acad. Sci. U.S.A. 100:13555-13560.
36. Keller PW, Adamson CS, Heymann JB, Freed EO, Steven AC. 2011. HIV-1 maturation inhibitor bevirimat stabilizes the immature Gag lattice. J. Virol. 85:1420-1428.
37. Zhou J, Yuan X, Dismuke D, Forshey BM, Lundquist C, Lee KH, Aiken C, Chen CH. 2004. Small-molecule inhibition of human immunodeficiency virus type 1 replication by specific targeting of the final step of virion maturation. J. Virol. 78:922-929.
38. Briggs JA, Simon MN, Gross I, Kräusslich HG, Fuller SD, Vogt VM, Johnson MC. 2004. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11:672-675.
39. Briggs JA, Grunewald K, Glass B, Forster F, Kräusslich HG, Fuller SD. 2006. The mechanism of HIV-1 core assembly:insights from threedimensional reconstructions of authentic virions. Structure 14:15-20.
40. Lanman J, Lam TT, Emmett MR, Marshall AG, Sakalian M, Prevelige PE, Jr. 2004. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 11:676-677.
41. Jin AJ, Nossal R. 1993. Topological mechanisms involved in the formation of clathrin-coated vesicles. Biophys. J. 65:1523-1537.
42. Purdy JG, Flanagan JM, Ropson IJ, Craven RC. 2009. Retroviral capsid assembly:a role for the CA dimer in initiation. J. Mol. Biol. 389:438-451.
43. Butan C, Winkler DC, Heymann JB, Craven RC, Steven AC. 2008. RSV capsid polymorphism correlates with polymerization efficiency and envelope glycoprotein content:implications that nucleation controls morphogenesis. J. Mol. Biol. 376:1168-1181.
44. Heymann JB, Belnap DM. 2007. Bsoft:image processing and molecular modeling for electron microscopy. J. Struct. Biol. 157:3-18.
45. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
46. Waki K, Durell SR, Soheilian F, Nagashima K, Butler SL, Freed EO. 2012. Structural and functional insights into the HIV-1 maturation inhibitor binding pocket. PLoS Pathog. 8:e1002997. doi:10.1371/journal.ppat.1002997.
47. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. 1986. Production of acquired immunodeficiency syndromeassociated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
48. Huang M, Orenstein JM, Martin MA, Freed EO. 1995. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818.
49. Heymann JB, Cardone G, Winkler DC, Steven AC. 2008. Computational resources for cryo-electron tomography in Bsoft. J. Struct. Biol. 161:232-242.
50. Cardone G, Grünewald K, Steven AC. 2005. A resolution criterion for electron tomography based on cross-validation. J. Struct. Biol. 151:117-129.
51. Purdy JG, Flanagan JM, Ropson IJ, Rennoll-Bankert KE, Craven RC. 2008. Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly. J. Virol. 82:5951-5961.
52. Purdy J. 2009. To assemble, or not to assemble:the initiation of retroviral capsid assembly. Ph.D. dissertation. Pennsylvania State University, Hershey, PA.
53. Blair WS, Cao J, Fok-Seang J, Griffin P, Isaacson J, Jackson RL, Murray E, Patick AK, Peng Q, Perros M, Pickford C, Wu H, Butler SL. 2009. New small-molecule inhibitor class targeting human immunodeficiency virus type 1 virion maturation. Antimicrob. Agents Chemother. 53:5080-5087.
54. Morellet N, Druillennec S, Lenoir C, Bouaziz S, Roques BP. 2005. Helical structure determined by NMR of the HIV-1 (345-392)Gag sequence, surrounding p2:implications for particle assembly and RNA packaging. Protein Sci. 14:375-386.
55. Gamble TR, Yoo S, Vajdos FF, von Schwedler UK, Worthylake DK, Wang H, McCutcheon JP, Sundquist WI, Hill CP. 1997. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278:849-853.
56. Nguyen AT, Feasley CL, Jackson KW, Nitz TJ, Salzwedel K, Air GM, Sakalian M. 2011. The prototype HIV-1 maturation inhibitor, bevirimat, binds to the CA-SP1 cleavage site in immature Gag particles. Retrovirology 8:101. doi:10.1186/1742-4690-8-101.
57. Steven AC, Carrascosa JL. 1979. Proteolytic cleavage and structural transformation:their relationship in bacteriophage T4 capsid maturation. J. Supramol. Struct. 10:1-11.
58. Plevka P, Battisti AJ, Junjhon J, Winkler DC, Holdaway HA, Keelapang P, Sittisombut N, Kuhn RJ, Steven AC, Rossmann MG. 2011. Maturation of flaviviruses starts from one or more icosahedrally independent nucleation centres. EMBO Rep. 12:602-606.