The role of capsid maturation on adenovirus priming for sequential uncoating

Journal of Biological Chemistry

Volumn 287, Issue 37, 2012, Pages 31582-31595

  Pérez Berná, Ana J ^a   Ortega Esteban, Alvaro ^a   Menéndez Conejero, Rosa ^a   Winkler, Dennis C ^c   Menéndez, Margarita ^b   Steven, Alasdair C ^c   Flint, S Jane ^d   De Pablo, Pedro J ^a   San Martín, Carmen ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

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

^d PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC CONDITIONS; BIOPHYSICAL TECHNIQUES; CORE PROTEINS; CRYO-ELECTRON TOMOGRAPHY; DNA RELEASE; ENDOSOMES; IN-VITRO; INTERNAL PRESSURE; PRECURSOR PROTEINS; PROTEOLYTIC PROCESSING; SHELL FRAGMENTS; STRESS CONDITION; STRESS LEVELS; STRUCTURAL STUDIES;

ELASTICITY;

VIRUSES;

CORE PROTEIN; VIRUS DNA;

ADENOVIRUS; ARTICLE; CONTROLLED STUDY; CROSS PRESENTATION; ELASTICITY; ELECTRON TOMOGRAPHY; ENDOSOME; IMMATURE VIRUS; MATURATION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; STRESS; VIRION; VIRUS CAPSID; VIRUS GENOME; VIRUS UNCOATING;

ADENOVIRIDAE; CAPSID; DNA, VIRAL; HEK293 CELLS; HUMANS; VIRUS INTERNALIZATION;

ADENOVIRIDAE; MIRIDAE;

EID: 84866056104     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.389957     Document Type: Article

References (66)

1. Leen, A. M., and Rooney, C. M. (2005) Adenovirus as an emerging pathogen in immunocompromised patients. Br. J. Haematol. 128, 135-144
2. Singh, R., and Kostarelos, K. (2009) Designer adenoviruses for nanomedicine and nanodiagnostics. Trends Biotechnol. 27, 220-229
3. Liu, H., Jin, L., Koh, S. B., Atanasov, I., Schein, S., Wu, L., and Zhou, Z. H. (2010) Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 329, 1038-1043
4. Silvestry, M., Lindert, S., Smith, J. G., Maier, O., Wiethoff, C. M., Nemerow, G. R., and Stewart, P. L. (2009) Cryoelectron microscopy structure of adenovirus type 2 temperature-sensitive mutant 1 reveals insight into the cell entry defect. J. Virol. 83, 7375-7383
5. Pérez-Berná, A. J., Marabini, R., Scheres, S. H., Menéndez-Conejero, R., Dmitriev, I. P., Curiel, D. T., Mangel, W. F., Flint, S. J., and San Martín, C. (2009) Structure and uncoating of immature adenovirus. J. Mol. Biol. 392, 547-557
6. Baniecki, M. L., McGrath, W. J., McWhirter, S. M., Li, C., Toledo, D. L., Pellicena, P., Barnard, D. L., Thorn, K. S., and Mangel, W. F. (2001) Interaction of the human adenovirus proteinase with its 11-amino acid cofactor pVIc. Biochemistry 40, 12349-12356
7. Chroboczek, J., Bieber, F., and Jacrot, B. (1992) The sequence of the genome of adenovirus type 5 and its comparison with the genome of adenovirus type 2. Virology 186, 280-285
8. Smith, J. G., Wiethoff, C. M., Stewart, P. L., and Nemerow, G. R. (2010) Adenovirus. Curr. Top. Microbiol. Immunol. 343, 195-224
9. Greber, U. F., Willetts, M., Webster, P., and Helenius, A. (1993) Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75, 477-486
10. Nakano, M. Y., Boucke, K., Suomalainen, M., Stidwill, R. P., and Greber, U. F. (2000) The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J. Virol. 74, 7085-7095
11. Lindert, S., Silvestry, M., Mullen, T. M., Nemerow, G. R., and Stewart, P. L. (2009) Cryoelectron microscopy structure of an adenovirus-integrin complex indicates conformational changes in both penton base and integrin. J. Virol. 83, 11491-11501
12. Puntener, D., Engelke, M. F., Ruzsics, Z., Strunze, S., Wilhelm, C., and Greber, U. F. (2011) Stepwise loss of fluorescent core protein V from human adenovirus during entry into cells. J. Virol. 85, 481-496
13. Wiethoff, C. M., Wodrich, H., Gerace, L., and Nemerow, G. R. (2005) Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol. 79, 1992-2000
14. Gastaldelli, M., Imelli, N., Boucke, K., Amstutz, B., Meier, O., and Greber, U. F. (2008) Infectious adenovirus type 2 transport through early but not late endosomes. Traffic 9, 2265-2278
15. Nociari, M., Ocheretina, O., Schoggins, J. W., and Falck-Pedersen, E. (2007) Sensing infection by adenovirus. Toll-like receptor-independent viral DNA recognition signals activation of the interferon regulatory factor 3 master regulator. J. Virol. 81, 4145-4157
16. Bremner, K. H., Scherer, J., Yi, J., Vershinin, M., Gross, S. P., and Vallee, R. B. (2009) Adenovirus transport via direct interaction of cytoplasmic dynein with the viral capsid hexon subunit. Cell Host Microbe 6, 523-535
17. Suomalainen, M., Nakano, M. Y., Keller, S., Boucke, K., Stidwill, R. P., and Greber, U. F. (1999) Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J. Cell Biol. 144, 657-672
18. Chatterjee, P. K., Vayda, M. E., and Flint, S. J. (1986) Adenoviral protein VII packages intracellular viral DNA throughout the early phase of infection. EMBO J. 5, 1633-1644
19. Greber, U. F., Webster, P., Weber, J., and Helenius, A. (1996) The role of the adenovirus protease on virus entry into cells. EMBO J. 15, 1766-1777
20. Greber, U. F., Suomalainen, M., Stidwill, R. P., Boucke, K., Ebersold, M. W., and Helenius, A. (1997) The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16, 5998-6007
21. Trotman, L. C., Mosberger, N., Fornerod, M., Stidwill, R. P., and Greber, U. F. (2001) Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 3, 1092-1100
22. Weber, J. M. (1999) in Adenoviruses: Basic Biology to Gene Therapy (Seth, P., ed) pp. 79-83, R. G. Landes, Austin, TX
23. Weber, J. (1976) Genetic analysis of adenovirus type 2 III. Temperature sensitivity of processing viral proteins. J. Virol. 17, 462-471
24. Rancourt, C., Keyvani-Amineh, H., Sircar, S., Labrecque, P., and Weber, J. M. (1995) Proline 137 is critical for adenovirus protease encapsidation and activation but not enzyme activity. Virology 209, 167-173
25. Cotten, M., and Weber, J. M. (1995) The adenovirus protease is required for virus entry into host cells. Virology 213, 494-502
26. San Martín, C. (2012) Latest insights on adenovirus structure and assembly. Viruses 4, 847-877
27. Seki, T., Dmitriev, I., Kashentseva, E., Takayama, K., Rots, M., Suzuki, K., and Curiel, D. T. (2002) Artificial extension of the adenovirus fiber shaft inhibits infectivity in coxsackievirus and adenovirus receptor-positive cell lines. J. Virol. 76, 1100-1108
28. Sanchez-Ruiz, J. M. (1992) Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry. Biophys. J. 61, 921-935
29. Carreira, A., Menéndez, M., Reguera, J., Almendral, J. M., and Mateu, M. G. (2004) In vitro disassembly of a parvovirus capsid and effect on capsid stability of heterologous peptide insertions in surface loops. J. Biol. Chem. 279, 6517-6525
30. Harris, A., Cardone, G., Winkler, D. C., Heymann, J. B., Brecher, M., White, J. M., and Steven, A. C. (2006) Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl. Acad. Sci. U.S.A. 103, 19123-19127
31. Mastronarde, D. N. (2005) Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51
32. Kremer, J. R., Mastronarde, D. N., and McIntosh, J. R. (1996) Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76
33. Agulleiro, J. I., and Fernandez, J. J. (2011) Fast tomographic reconstruction on multicore computers. Bioinformatics 27, 582-583
34. Frangakis, A. S., and Hegerl, R. (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 135, 239-250
35. Heymann, J. B., Cardone, G., Winkler, D. C., and Steven, A. C. (2008) Computational resources for cryoelectron tomography in Bsoft. J. Struct. Biol. 161, 232-242
36. Scheres, S. H., Núñez-Ramírez, R., Sorzano, C. O., Carazo, J. M., and Marabini, R. (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc. 3, 977-990
37. Scheres, S. H., Melero, R., Valle, M., and Carazo, J. M. (2009) Averaging of electron subtomograms and random conical tilt reconstructions through likelihood optimization. Structure 17, 1563-1572
38. Ortega-Esteban, A., Horcas, I., Hernando-Pérez, M., Ares, P., Pérez- Berná, A. J., San Martín, C., Carrascosa, J. L., de Pablo, P. J., and Gómez- Herrero, J. (2012) Minimizing tip-sample forces in jumping mode atomic force microscopy in liquid. Ultramicroscopy 114, 56-61
39. Sader, J. E., Chon, J. W., and Mulvaney, P. (1999) Calibration of rectangular atomic force microscope cantilevers. Rev. Sci. Instrum. 70, 3967-3969
40. Zink, M., and Grubmüller, H. (2009) Mechanical properties of the icosahedral shell of southern bean mosaic virus. A molecular dynamics study. Biophys. J. 96, 1350-1363
41. Horcas, I., Fernández, R., Gómez-Rodríguez, J. M., Colchero, J., Gómez-Herrero, J., and Baro, A. M. (2007) WSXM. A software for scanning probe microscopy and a tool for nanotechnology. Rev. Sci. Instrum. 78, 013705
42. Ihnat, P. M., Vellekamp, G., Obenauer-Kutner, L. J., Duan, J., Han, M. A., Witchey-Lakshmanan, L. C., and Grace, M. J. (2005) Comparative thermal stabilities of recombinant adenoviruses and hexon protein. Biochim. Biophys. Acta 1726, 138-151
43. Rexroad, J., Evans, R. K., and Middaugh, C. R. (2006) Effect of pH and ionic strength on the physical stability of adenovirus type 5. J. Pharm. Sci. 95, 237-247
44. Rexroad, J., Martin, T. T., McNeilly, D., Godwin, S., and Middaugh, C. R. (2006) Thermal stability of adenovirus type 2 as a function of pH. J. Pharm. Sci. 95, 1469-1479
45. Rexroad, J., Wiethoff, C. M., Green, A. P., Kierstead, T. D., Scott, M. O., and Middaugh, C. R. (2003) Structural stability of adenovirus type 5. J. Pharm. Sci. 92, 665-678
46. Lozach, P. Y., Huotari, J., and Helenius, A. (2011) Late-penetrating viruses. Curr. Opin. Virol. 1, 35-43
47. Zandi, R., and Reguera, D. (2005) Mechanical properties of viral capsids. Phys. Rev. E Stat. Nonlin. Soft. Matter Phys. 72, 021917
48. De Pablo, P. J., Schaap, I. A., MacKintosh, F. C., and Schmidt, C. F. (2003) Deformation and collapse of microtubules on the nanometer scale. Phys. Rev. Lett. 91, 981011-981014
49. Carrasco, C., Carreira, A., Schaap, I. A., Serena, P. A., Gómez-Herrero, J., Mateu, M. G., and de Pablo, P. J. (2006) DNA-mediated anisotropic mechanical reinforcement of a virus. Proc. Natl. Acad. Sci. U.S.A. 103, 13706-13711
50. Mangel, W. F., McGrath, W. J., Toledo, D. L., and Anderson, C. W. (1993) Viral DNA and a viral peptide can act as cofactors of adenovirus virion proteinase activity. Nature 361, 274-275
51. Hannan, C., Raptis, L. H., Déry, C. V., and Weber, J. (1983) Biological and structural studies with an adenovirus type 2 temperature- sensitive mutant defective for uncoating. Intervirology 19, 213-223
52. Galisteo, M. L., and King, J. (1993) Conformational transformations in the protein lattice of phage P22 procapsids. Biophys. J. 65, 227-235
53. Ross, P. D., Conway, J. F., Cheng, N., Dierkes, L., Firek, B. A., Hendrix, R. W., Steven, A. C., and Duda, R. L. (2006) A free energy cascade with locks drives assembly and maturation of bacteriophage HK97 capsid. J. Mol. Biol. 364, 512-525
54. Huang, R. K., Khayat, R., Lee, K. K., Gertsman, I., Duda, R. L., Hendrix, R. W., and Johnson, J. E. (2011) The Prohead-I structure of bacteriophage HK97. Implications for scaffold-mediated control of particle assembly and maturation. J. Mol. Biol. 408, 541-554
55. Teschke, C. M., McGough, A., and Thuman-Commike, P. A. (2003) Penton release from P22 heat-expanded capsids suggests importance of stabilizing penton-hexon interactions during capsid maturation. Biophys. J. 84, 2585-2592
56. Wodrich, H., Guan, T., Cingolani, G., Von Seggern, D., Nemerow, G., and Gerace, L. (2003) Switch from capsid protein import to adenovirus assembly by cleavage of nuclear transport signals. EMBO J. 22, 6245-6255
57. Russell, W. C., and Precious, B. (1982) Nucleic acid-binding properties of adenovirus structural polypeptides. J. Gen. Virol. 63, 69-79
58. Johnson, J. E., and Chiu, W. (2007) DNA packaging and delivery machines in tailed bacteriophages. Curr. Opin. Struct. Biol. 17, 237-243
59. Strunze, S., Engelke, M. F., Wang, I. H., Puntener, D., Boucke, K., Schleich, S., Way, M., Schoenenberger, P., Burckhardt, C. J., and Greber, U. F. (2011) Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 10, 210-223
60. Hogle, J. M. (2002) Poliovirus cell entry. Common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56, 677-702
61. Burckhardt, C. J., Suomalainen, M., Schoenenberger, P., Boucke, K., Hemmi, S., and Greber, U. F. (2011) Drifting motions of the adenovirus receptor CAR and immobile integrins initiate virus uncoating and membrane lytic protein exposure. Cell Host Microbe 10, 105-117
62. Chatterjee, P. K., Vayda, M. E., and Flint, S. J. (1985) Interactions among the three adenovirus core proteins. J. Virol. 55, 379-386
63. Roos, W. H., Radtke, K., Kniesmeijer, E., Geertsema, H., Sodeik, B., and Wuite, G. J. (2009) Scaffold expulsion and genome packaging trigger stabilization of herpes simplex virus capsids. Proc. Natl. Acad. Sci. U.S.A. 106, 9673-9678
64. Baclayon, M., Shoemaker, G. K., Uetrecht, C., Crawford, S. E., Estes, M. K., Prasad, B. V., Heck, A. J., Wuite, G. J., and Roos, W. H. (2011) Prestress strengthens the shell of Norwalk virus nanoparticles. Nano. Lett. 11, 4865-4869
65. Roos, W. H., Gertsman, I., May, E. R., Brooks, C. L., 3rd, Johnson, J. E., and Wuite, G. J. (2012) Mechanics of bacteriophage maturation. Proc. Natl. Acad. Sci. U.S.A. 109, 2342-2347
66. Gelbart, W. M., and Knobler, C. M. (2009) Virology. Pressurized viruses. Science 323, 1682-1683