Differential protein partitioning within the herpesvirus tegument and envelope underlies a complex and variable virion architecture

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 17, 2013, Pages

  Bohannon, Kevin Patrick ^a   Jun, Yonggun ^b   Gross, Steven P ^b   Smith, Gregory Allan ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Asymmetry; Heterogeneity; Point spread function; Pseudorabies; Virus

Indexed keywords

VIRUS PROTEIN;

ARTICLE; HERPES VIRUS; INTEGUMENT; NONHUMAN; PRIORITY JOURNAL; VIRION; VIRUS ENVELOPE; VIRUS PARTICLE;

ANIMALS; CELL LINE; CHROMOSOMES, ARTIFICIAL, BACTERIAL; HERPESVIRUS 1, SUID; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTAGENESIS; SWINE; VIRAL STRUCTURAL PROTEINS; VIRION;

HERPESVIRIDAE; MIRIDAE;

EID: 84876878143     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1221896110     Document Type: Article

References (72)

1. Szilágyi JF, Cunningham C (1991) Identification and characterization of a novel non-infectious herpes simplex virus-related particle. J Gen Virol 72(Pt 3):661-668.
2. Zhou ZH, Chen DH, Jakana J, Rixon FJ, Chiu W (1999) Visualization of tegument-capsid interactions and DNAin intact herpes simplex virus type 1 virions. J Virol 73(4):3210-3218.
3. Cardone G, et al. (2012) The UL36 tegument protein of herpes simplex virus 1 has a composite binding site at the capsid vertices. J Virol 86(8):4058-4064.
4. Zhou ZH, et al. (2000) Seeing the herpesvirus capsid at 8.5 Å. Science 288(5467): 877-880.
5. Paredes AM, et al. (1993) Three-dimensional structure of a membrane-containing virus. Proc Natl Acad Sci USA 90(19):9095-9099.
6. Zhang W, et al. (2002) Placement of the structural proteins in Sindbis virus. J Virol 76(22):11645-11658.
7. Zhang R, et al. (2011) 4.4 Å cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. EMBO J 30(18):3854-3863.
8. Grünewald K, et al. (2003) Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302(5649):1396-1398.
9. Spear PG, Longnecker R (2003) Herpesvirus entry: An update. J Virol 77(19): 10179-10185.
10. Batterson W, Roizman B (1983) Characterization of the herpes simplex virion-associated factor responsible for the induction of alpha genes. J Virol 46(2):371-377.
11. Ace CI, McKee TA, Ryan JM, Cameron JM, Preston CM (1989) Construction and characterization of a herpes simplex virus type 1 mutant unable to transinduce immediate-early gene expression. J Virol 63(5):2260-2269.
12. Krautwald M, Fuchs W, Klupp BG, Mettenleiter TC (2009) Translocation of incoming pseudorabies virus capsids to the cell nucleus is delayed in the absence of tegument protein pUL37. J Virol 83(7):3389-3396.
13. Schipke J, et al. (2012) The C terminus of the large tegument protein pUL36 contains multiple capsid binding sites that function differently during assembly and cell entry of herpes simplex virus. J Virol 86(7):3682-3700.
14. Abaitua F, Hollinshead M, Bolstad M, Crump CM, O'Hare P (2012) A Nuclear localization signal in herpesvirus protein VP1-2 is essential for infection via capsid routing to the nuclear pore. J Virol 86(17):8998-9014.
15. Mettenleiter TC, Klupp BG, Granzow H (2009) Herpesvirus assembly: An update. Virus Res 143(2):222-234.
16. Kelly BJ, Fraefel C, Cunningham AL, Diefenbach RJ (2009) Functional roles of the tegument proteins of herpes simplex virus type 1. Virus Res 145(2):173-186.
17. Meckes DG, Jr., Wills JW (2008) Structural rearrangement within an enveloped virus upon binding to the host cell. J Virol 82(21):10429-10435.
18. Maurer UE, Sodeik B, Grünewald K (2008) Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc Natl Acad Sci USA 105(30):10559-10564.
19. Newcomb WW, Brown JC (2009) Time-dependent transformation of the herpesvirus tegument. J Virol 83(16):8082-8089.
20. Smith GA, Enquist LW (2000) A self-recombining bacterial artificial chromosome and its application for analysis of herpesvirus pathogenesis. Proc Natl Acad Sci USA 97(9): 4873-4878.
21. Trus BL, et al. (1995) Herpes simplex virus capsids assembled in insect cells infected with recombinant baculoviruses: structural authenticity and localization of VP26. J Virol 69(11):7362-7366.
22. Zhou ZH, et al. (1995) Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat Struct Biol 2(11):1026-1030.
23. Zaichick SV, et al. (2013) The Herpesvirus VP1/2 protein is an effector of dynein-mediated capsid transport and neuroinvasion. Cell Host Microbe 13(2):193-203.
24. Thurlow JK, et al. (2005) The herpes simplex virus type 1 DNA packaging protein UL17 is a virion protein that is present in both the capsid and the tegument compartments. J Virol 79(1):150-158.
25. Fuchs W, Klupp BG, Granzow H, Mettenleiter TC (2004) Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J Virol 78(21):11879-11889.
26. del Rio T, Ch'ng TH, Flood EA, Gross SP, Enquist LW (2005) Heterogeneity of a fluorescent tegument component in single pseudorabies virus virions and enveloped axonal assemblies. J Virol 79(7):3903-3919.
27. Kaelin K, Dezélée S, Masse MJ, Bras F, Flamand A (2000) The UL25 protein of pseudorabies virus associates with capsids and localizes to the nucleus and to microtubules. J Virol 74(1):474-482.
28. Newcomb WW, et al. (2001) The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J Virol 75(22):10923-10932.
29. Toropova K, Huffman JB, Homa FL, Conway JF (2011) The herpes simplex virus 1 UL17 protein is the second constituent of the capsid vertex-specific component required for DNA packaging and retention. J Virol 85(15):7513-7522.
30. Cockrell SK, Huffman JB, Toropova K, Conway JF, Homa FL (2011) Residues of the UL25 protein of herpes simplex virus that are required for its stable interaction with capsids. J Virol 85(10):4875-4887.
31. Conway JF, et al. (2010) Labeling and localization of the herpes simplex virus capsid protein UL25 and its interaction with the two triplexes closest to the penton. J Mol Biol 397(2):575-586.
32. Charpilienne A, et al. (2001) Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J Biol Chem 276(31):29361-29367.
33. Bohannon KP, Sollars PJ, Pickard GE, Smith GA (2012) Fusion of a fluorescent protein to the pUL25 minor capsid protein of pseudorabies virus allows live-cell capsid imaging with negligible impact on infection. J Gen Virol 93(Pt 1):124-129.
34. Schrag JDJ, Prasad BVBV, Rixon FJF, Chiu WW (1989) Three-dimensional structure of the HSV1 nucleocapsid. Cell 56(4):651-660.
35. McLauchlan J (1997) The abundance of the herpes simplex virus type 1 UL37 tegument protein in virus particles is closely controlled. J Gen Virol 78(Pt 1):189-194.
36. Hoffman MT, Sheung J, Selvin PR (2011) Fluorescence imaging with one nanometer accuracy: In vitro and in vivo studies of molecular motors. Methods Mol Biol 778: 33-56.
37. Booy FP, et al. (1994) Finding a needle in a haystack: Detection of a small protein (the 12-kDa VP26) in a large complex (the 200-MDa capsid of herpes simplex virus). Proc Natl Acad Sci USA 91(12):5652-5656.
38. Trus BL, et al. (2007) Allosteric signaling and a nuclear exit strategy: Binding of UL25/UL17 heterodimers to DNA-Filled HSV-1 capsids. Mol Cell 26(4):479-489.
39. Spear PG, Roizman B (1967) Buoyant density of herpes simplex virus in solutions of caesium chloride. Nature 214(5089):713-714.
40. Scrivano L, Sinzger C, Nitschko H, Koszinowski UH, Adler B (2011) HCMV spread and cell tropism are determined by distinct virus populations. PLoS Pathog 7(1):e1001256.
41. Borza CM, Hutt-Fletcher LM (2002) Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat Med 8(6):594-599.
42. Morgan C, Rose HM, Mednis B (1968) Electron microscopy of herpes simplex virus. I. Entry. J Virol 2(5):507-516.
43. Vernon SK, Lawrence WC, Long CA, Rubin BA, Sheffield JB (1982) Morphological components of herpesvirus. IV. Ultrastructural features of the envelope and tegument. J Ultrastruct Res 81(2):163-171.
44. Schmid MF, et al. (2012) A tail-like assembly at the portal vertex in intact herpes simplex type-1 virions. PLoS Pathog 8(10):e1002961.
45. Clarke RW, et al. (2007) Two-color fluorescence analysis of individual virions determines the distribution of the copy number of proteins in herpes simplex virus particles. Biophys J 93(4):1329-1337.
46. Luxton GWG, et al. (2005) Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc Natl Acad Sci USA 102(16):5832-5837.
47. Handler CG, Eisenberg RJ, Cohen GH (1996) Oligomeric structure of glycoproteins in herpes simplex virus type 1. J Virol 70(9):6067-6070.
48. Coller KE, Lee JI-H, Ueda A, Smith GA (2007) The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J Virol 81(21):11790-11797.
49. Leelawong M, Lee JI, Smith GA (2012) Nuclear egress of pseudorabies virus capsids is enhanced by a subspecies of the large tegument protein that is lost upon cytoplasmic maturation. J Virol 86(11):6303-6314.
50. Michael K, Böttcher S, Klupp BG, Karger A, Mettenleiter TC (2006) Pseudorabies virus particles lacking tegument proteins pUL11 or pUL16 incorporate less full-length pUL36 than wild-type virus, but specifically accumulate a pUL36 N-terminal fragment. J Gen Virol 87(Pt 12):3503-3507.
51. Chang JT, Schmid MF, Rixon FJ, Chiu W (2007) Electron cryotomography reveals the portal in the herpesvirus capsid. J Virol 81(4):2065-2068.
52. Klupp BGB, Fuchs WW, Granzow HH, Nixdorf RR, Mettenleiter TCT (2002) Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J Virol 76(6):3065-3071.
53. Vittone V, et al. (2005) Determination of interactions between tegument proteins of herpes simplex virus type 1. J Virol 79(15):9566-9571.
54. Wolfstein A, et al. (2006) The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7(2):227-237.
55. Mettenleiter TC (2004) Budding events in herpesvirus morphogenesis. Virus Res 106(2):167-180.
56. Cardone G, et al. (2007) Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361(2):426-434.
57. Deng B, O'Connor CM, Kedes DH, Zhou ZH (2007) Direct visualization of the putative portal in the Kaposi's sarcoma-associated herpesvirus capsid by cryoelectron tomography. J Virol 81(7):3640-3644.
58. Meckes DG, Jr., Wills JW (2007) Dynamic interactions of the UL16 tegument protein with the capsid of herpes simplex virus. J Virol 81(23):13028-13036.
59. Svobodova S, Bell S, Crump CM (2012) Analysis of the interaction between the essential herpes simplex virus 1 tegument proteins VP16 and VP1/2. J Virol 86(1):473-483.
60. Ko DH, Cunningham AL, Diefenbach RJ (2010) The major determinant for addition of tegument protein pUL48 (VP16) to capsids in herpes simplex virus type 1 is the presence of the major tegument protein pUL36 (VP1/2). J Virol 84(3):1397-1405.
61. Fuchs W, Granzow H, Klupp BG, Kopp M, Mettenleiter TC (2002) The UL48 tegument protein of pseudorabies virus is critical for intracytoplasmic assembly of infectious virions. J Virol 76(13):6729-6742.
62. Scholtes LD, Yang K, Li LX, Baines JD (2010) The capsid protein encoded by U(L)17 of herpes simplex virus 1 interacts with tegument protein VP13/14. J Virol 84(15):7642-7650.
63. Radtke K, et al. (2010) Plus-and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog 6(7):e1000991.
64. Klupp BG, Nixdorf R, Mettenleiter TC (2000) Pseudorabies virus glycoprotein M inhibits membrane fusion. J Virol 74(15):6760-6768.
65. Koyano S, Mar E-C, Stamey FR, Inoue N (2003) Glycoproteins M and N of human herpesvirus 8 form a complex and inhibit cell fusion. J Gen Virol 84(Pt 6):1485-1491.
66. Chojnacki J, et al. (2012) Maturation-dependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science 338(6106):524-528.
67. Tischer BK, von Einem J, Kaufer B, Osterrieder N (2006) Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40(2):191-197.
68. Smith GA, Gross SP, Enquist LW (2001) Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc Natl Acad Sci USA 98(6):3466-3470.
69. Antinone SE, Zaichick SV, Smith GA (2010) Resolving the assembly state of herpes simplex virus during axon transport by live-cell imaging. J Virol 84(24):13019-13030.
70. Wand MP (1997) Data-based choice of histogram bin width. Am Stat 51(1):59-64.
71. Ruusuvuori P, et al. (2010) Evaluation of methods for detection of fluorescence labeled subcellular objects in microscope images. BMC Bioinformatics 11:248.
72. Otsu N (1979) A threshold selection method form gray-level histograms. IEEE T Syst Man Cyb 9(1):62-66.