Herpesviruses remodel host membranes for virus egress

Nature Reviews Microbiology

Volumn 9, Issue 5, 2011, Pages 382-394

  Johnson, David C ^a   Baines, Joel D ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; LAMIN A; LAMIN B; LAMIN C;

ARTICLE; EPSTEIN BARR VIRUS; HERPES SIMPLEX VIRUS; HERPES VIRUS; HOST; HUMAN CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 8; NONHUMAN; NUCLEAR LAMINA; PRIORITY JOURNAL; VARICELLA ZOSTER VIRUS; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS RELEASE;

ANIMALS; CELL MEMBRANE; EPITHELIAL CELLS; HERPESVIRIDAE; HERPESVIRIDAE INFECTIONS; HUMANS; VIRUS RELEASE;

DNA VIRUSES; HERPESVIRIDAE; MIRIDAE;

EID: 79954599465     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2559     Document Type: Article

References (267)

1. Spear, P. G. & Longnecker, R. Herpesvirus entry: an update. J. Virol. 77, 10179-10185 (2003). (Pubitemid 37129662)
2. Heldwein, E. E. & Krummenacher, C. Entry of herpesviruses into mammalian cells. Cell. Mol. Life Sci. 65, 1653-1668 (2008).
3. Baines, J. D. & Duffy, C. in Alpha Herpesviruses: Pathogenesis, Molecular Biology and Infection Control (ed. Sandri-Goldin, R. M.) 175-204 (Caister Scientific, Norfolk, 2006).
4. Mettenleiter, T. C. Herpesvirus assembly and egress. J Virol. 76, 1537-1547 (2002). (Pubitemid 34094600)
5. Mettenleiter, T. C, Klupp, B. G. & Granzow, H. Herpesvirus assembly: an update. Virus Res. 143, 222-234 (2009).
6. Sanchez, V, Sztul, E. & Britt, W. J. Human cytomegalovirus pp28 (UL99) localizes to a cytoplasmic compartment which overlaps the endoplasmic reticulum-Golgi-intermediate compartment. J. Virol. 74, 3842-3851 (2000). (Pubitemid 30180326)
7. Das, S., Vasanji, A. & Pellett, P. E. Three-dimensional structure of the human cytomegalovirus cytoplasmic virion assembly complex includes a reoriented secretory apparatus. J. Virol. 81, 11861-11869 (2007). (Pubitemid 47623818)
8. Buchkovich, N. J., Maguire, T. G. & Alwine, J. C. Role of the endoplasmic reticulum chaperone BiP, SUN domain proteins, and dynein in altering nuclear morphology during human cytomegalovirus infection. J. Virol. 84, 7005-7017 (2010).
9. Hofemeister, H. & O'Hare, P. Nuclear pore composition and gating in herpes simplex virus-infected cells. J. Virol. 82, 8392-8399 (2008).
10. Johnson, D. C. & Huber, M. T. Directed egress of animal viruses promotes cell-to-cell spread. J. Virol. 76, 1-8 (2002). (Pubitemid 33138986)
11. Curanovic, D. & Enquist, L. Directional transneuronal spread of α-herpesvirus infection. Future Virol. 4, 591 (2009).
12. L31 gene of herpes simplex virus 1: construction and phenotype in infected cells. J. Virol. 71, 8307-8315 (1997). (Pubitemid 27446407)
13. L34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J. Virol. 75, 8803-8817 (2001). (Pubitemid 32768984)
14. L34 gene product is required for viral envelopment. J. Virol. 74, 117-129 (2000). (Pubitemid 30002890)
15. Chang, Y E. & Roizman, B. The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. J. Virol. 67, 6348-6356 (1993). (Pubitemid 23309098)
16. Reynolds, A. E., Wills, E. G., Roller, R. J., Ryckman, B. J. & Baines, J. D. Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J. Virol. 76, 8939-8952 (2002). (Pubitemid 34864088)
17. McGeoch, D. J. et al. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen. Virol. 69, 1531-1574 (1988).
18. Shiba, C. et al. The UL34 gene product of herpes simplex virus type 2 is a tail-anchored type II membrane protein that is significant for virus envelopment. J. Gen. Virol. 81, 2397-2405 (2000).
19. Fuchs, W., Granzow, H., Klupp, B. G., Kopp, M. & Mettenleiter, T. C. The UL48 tegument protein of pseudorabies virus is critical for intracytoplasmic assembly of infectious virions. J. Virol. 76, 6729-6742 (2002). (Pubitemid 34633539)
20. Klupp, B. G. et al. Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc. Natl Acad. Sci. USA 104, 7241-7246 (2007). (Pubitemid 47186039)
21. Roller, R. J., Bjerke, S. L, Haugo, A. C. & Hanson, S. Analysis of a charge cluster mutation of herpes simplex virus type 1 UL34 and its extragenic suppressor suggests a novel interaction between pUL34 and pUL31 that is necessary for membrane curvature around capsids. J. Virol. 84, 3921-3934 (2010).
22. Dechat, T. et al. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22, 832-853 (2008). (Pubitemid 351482836)
23. L34. J. Virol. 78, 5564-5575 (2004). (Pubitemid 38661643)
24. Simpson-Holley, M., Colgrove, R. C, Nalepa, G., Harper, J. W. & Knipe, D. M. Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. J. Virol. 79, 12840-12851 (2005). (Pubitemid 41433203)
25. Bjerke, S. L. & Roller, R. J. Roles for herpes simplex virus type 1 UL34 and US3 proteins in disrupting the nuclear lamina during herpes simplex virus type 1 egress. Virology 347, 261-276 (2006).
26. Mou, F., Forest, T. & Baines, J. D. US3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. J. Virol. 81, 6459-6470 (2007). (Pubitemid 46878051)
27. Park, R. & Baines, J. D. Herpes simplex virus type 1 infection induces activation and recruitment of protein kinase C to the nuclear membrane and increased phosphorylation of lamin B. J. Virol. 80, 494-504 (2006).
28. Leach, N. R. & Roller, R. J. Significance of host cell kinases in herpes simplex virus type 1 egress and lamin-associated protein disassembly from the nuclear lamina. Virology 406, 127-137 (2010).
29. Muranyi, W., Haas, J., Wagner, M., Krohne, G. & Koszinowski, U. H. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 297, 854-857 (2002). (Pubitemid 34839639)
30. Lee, C. P. et al. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J. Virol. 82, 11913-11926 (2008).
31. Hamirally, S. et al. Viral mimicry of Cdc2/cyclin-dependent kinase 1 mediates disruption of nuclear lamina during human cytomegalovirus nuclear egress. PLoS Pathog. 5, e1000275 (2009).
32. Gershburg, E., Raffa, S., Torrisi, M. R. & Pagano, J. S. Epstein-Barr virus-encoded protein kinase (BGLF4) is involved in production of infectious virus. J. Virol. 81, 5407-5412 (2007). (Pubitemid 46744449)
33. Krosky, P. M., Baek, M. C. & Coen, D. M. The human cytomegalovirus UL97 protein kinase, an antiviral drug target, is required at the stage of nuclear egress. J. Virol. 77, 905-914 (2003). (Pubitemid 36055512)
34. Cano-Monreal, G. L., Wylie, K. M., Cao, F, Tavis, J. E. & Morrison, L. A. Herpes simplex virus 2 UL13 protein kinase disrupts nuclear lamins. Virology 392, 137-147 (2009).
35. Marschall, M. et al. Cellular p32 recruits cytomegalovirus kinase pUL97 to redistribute the nuclear lamina. J. Biol. Chem. 280, 33357-33367 (2005). (Pubitemid 41397133)
36. Meng, Q., Hagemeier, S. R., Kuny, C. V., Kalejta, R. F & Kenney, S. C. Simian virus 40 T/t antigens and lamin A/C small interfering RNA rescue the phenotype of an Epstein-Barr virus protein kinase (BGLF4) mutant. J. Virol. 84, 4524-4533 (2010).
37. Milbradt, J., Webel, R., Auerochs, S., Sticht, H. & Marschall, M. Novel mode of phosphorylation-triggered reorganization of the nuclear lamina during nuclear egress of human cytomegalovirus. J. Biol. Chem. 285, 13979-13989 (2010).
38. Mou, F, Wills, E. G., Park, R. & Baines, J. D. Effects of lamin A/C, B1 and viral US3 kinase activity on viral infectivity, virion egress, and targeting the herpes simplex virus UL34-encoded protein to the inner nuclear membrane. J. Virol. 82, 8094-8104 (2008).
39. L34 gene products promote the late maturation of viral replication compartments to the nuclear periphery. J. Virol. 78, 5591-5600 (2004). (Pubitemid 38661646)
40. Leach, N. et al. Emerin is hyperphosphorylated and redistributed in herpes simplex virus type 1-infected cells in a manner dependent on both UL34 and US3. J. Virol. 81, 10792-10803 (2007). (Pubitemid 47463352)
41. Morris, J., Hofemeister, H. & O'Hare, P. Herpes simplex virus infection induces phosphorylation and delocalisation of emerin, a key inner nuclear membrane protein. J. Virol. 81, 4429-4437 (2007). (Pubitemid 46668640)
42. Roizman, B. & Furlong, D. in Comprehensive Virology (eds Fraenkel-Conrat, H. & Wagner, R. R.) 229-403 (Plenum, New York, 1974).
43. Thurlow, J. K., Murphy, M., Stow, N. D. & Preston, V. G. Herpes simplex virus type 1 DNA-packaging protein UL17 is required for efficient binding of UL25 to capsids. J. Virol. 80, 2118-2126 (2006). (Pubitemid 43271519)
44. Trus, B. L. et al. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol. Cell 26, 479-489 (2007). (Pubitemid 46765180)
45. L 17 gene encodes virion tegument proteins that are required for cleavage and packaging of viral DNA. J. Virol. 72, 3779-3788 (1998). (Pubitemid 28188676)
46. McNab, A. R. et al. The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J. Virol. 72, 1060-1070 (1998).
47. Klupp, B. G., Granzow, H., Keil, G. M. & Mettenleiter, T. C. The capsid-associated UL25 protein of the alphaherpesvirus pseudorabies virus is nonessential for cleavage and encapsidation of genomic DNA but is required for nuclear egress of capsids. J. Virol. 80, 6235-6246 (2006). (Pubitemid 43927426)
48. Naldinho-Souto, R., Browne, H. & Minson, T. Herpes simplex virus tegument protein VP16 is a component of primary enveloped virions. J. Virol. 80, 2582-2584 (2006). (Pubitemid 43271564)
49. Padula, M. E., Sydnor, M. L. & Wilson, D. W. Isolation and preliminary characterization of herpes simplex virus 1 primary enveloped virions from the perinuclear space. J. Virol. 83, 4757-4765 (2009).
50. Baines, J. D., Jacob, R. J., Simmerman, L. & Roizman, B. The herpes simplex virus 1 UL11 proteins are associated with cytoplasmic and nuclear membranes and with nuclear bodies of infected cells. J. Virol. 69, 825-833 (1995).
51. Read, G. S. & Patterson, M. Packaging of the virion host shutoff (Vhs) protein of herpes simplex virus: two forms of the Vhs polypeptide are associated with intranuclear B and C capsids, but only one is associated with enveloped virions. J. Virol. 81, 1148-1161 (2007). (Pubitemid 46167837)
52. Granzow, H. et al. Egress of alphaherpesviruses: comparative ultrastructural study. J. Virol. 75, 3675-3684 (2001). (Pubitemid 32246377)
53. Baines, J. D., Hsieh, C. E., Wills, E., Mannella, C. & Marko, M. Electron. tomography of nascent herpes simplex virus virions. J. Virol. 81, 2726-2735 (2007). (Pubitemid 46447037)
54. Torrisi, M. R., Di Lazzaro, C, Pavan, A., Pereira, L & Campadelli-Fiume, G. Herpes simplex virus envelopment and maturation studied by fracture label. J. Virol. 66, 554-561 (1992).
55. Baines, J. D., Wills, E., Jacob, R. J., Pennington, J. & Roizman, B. Glycoprotein M of herpes simplex virus 1 is incorporated into virions during budding at the inner nuclear membrane. J Virol. 81, 800-812 (2007). (Pubitemid 46067906)
56. Farnsworth, A. et al. Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane. Proc. Natl Acad. Sci. USA 104, 10187-10192 (2007). (Pubitemid 47175284)
57. Stannard, L. M., Himmelhoch, S. & Wynchank, S. Intra-nuclear localization of two envelope proteins, gB and gD, of herpes simplex virus. Arch. Virol. 141, 505-524 (1996). (Pubitemid 126706512)
58. L34 gene products of herpes simplex virus 1 are required for optimal localization of viral glycoproteins D and M to the inner nuclear membranes of infected cells. J. Virol. 83, 4800-4809 (2009).
59. Klupp, B., Altenschmidt, J., Granzow, H., Fuchs, W. & Mettenleiter, T C. Glycoproteins required for entry are not necessary for egress of pseudorabies virus. J. Virol. 82, 6299-6309 (2008). (Pubitemid 351875109)
60. Fuchs, W., Klupp, B. G., Granzow, H., Osterrieder, N. & Mettenleiter, T. C. The interacting UL31 and UL34 gene products of pseudorabies virus are involved in egress from the host-cell nucleus and represent components of primary enveloped but not mature virions. J. Virol. 76, 364-378 (2002). (Pubitemid 33139021)
61. Skepper, J. N., Whiteley, A., Browne, H. & Minson, A. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment-< deenvelopment-< reenvelopment pathway. J Virol. 75, 5697-5702 (2001). (Pubitemid 32488165)
62. Hannah, B. P. et al. Herpes simplex virus glycoprotein B associates with target membranes via its fusion loops. J. Virol. 83, 6825-6836 (2009).
63. Ryckman, B. J. & Roller, R. J. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. J. Virol. 78, 399-412 (2004). (Pubitemid 37549751)
64. Wright, C. C. et al. Fusion between perinuclear virions and the outer nuclear membrane requires the fusogenic activity of herpes simplex virus gB. J. Virol. 83, 11847-11856 (2009).
65. Krishnan, H. H., Sharma-Walia, N., Zeng, L, Gao, S. J. & Chandran, B. Envelope glycoprotein gB of Kaposi's sarcoma-associated herpesvirus is essential for egress from infected cells. J. Virol. 79, 10952-10967 (2005). (Pubitemid 41170637)
66. Lee, S. K. & Longnecker, R. The Epstein-Barr virus glycoprotein 110 carboxy-terminal tail domain is essential for lytic virus replication. J. Virol. 71, 4092-4097 (1997). (Pubitemid 27172426)
67. Ruel, N., Zago, A. & Spear, P. G. Alanine substitution of conserved residues in the cytoplasmic tail of herpes simplex virus gB can enhance or abolish cell fusion activity and viral entry. Virology 346, 229-237 (2006). (Pubitemid 43254713)
68. Wisner, T. W. et al. Herpesvirus gB-induced fusion between the virion envelope and outer nuclear membrane during virus egress is regulated by the viral US3 kinase. J. Virol. 83, 3115-3126 (2009).
69. S3-encoded kinase regulates localization of the nuclear envelopment complex and egress of nucleocapsids. J. Virol. 83, 5181-5191 (2009).
70. Ruyechan, W. T, Morse, L. S., Knipe, D. M. & Roizman, B. Molecular genetics of herpes simplex virus. II. Mapping of the major viral glycoproteins and of the genetic loci specifying the social behavior of infected cells. J. Virol. 29, 677-697 (1979). (Pubitemid 9098437)
71. Pogue-Geile, K. L., Lee, G. T., Shapira, S. K. & Spear, P. G. Fine mapping of mutations in the fusion-inducing MP strain of herpes simplex virus type 1. Virology 136, 100-109 (1984). (Pubitemid 14089591)
72. L20 gene of herpes simplex virus 1 encodes a function necessary for viral egress. J. Virol. 65, 6414-6424 (1991).
73. Foster, T P., Melancon, J. M., Baines, J. D. & Kousoulas, K. G. The herpes simplex virus type 1 UL20 protein modulates membrane fusion events during cytoplasmic virion morphogenesis and virus-induced cell fusion. J. Virol. 78, 5347-5357 (2004). (Pubitemid 38581485)
74. Hutchinson, L. & Johnson, D. C. Herpes simplex virus glycoprotein K promotes egress of virus particles. J. Virol. 69, 5401-5413 (1995).
75. Jayachandra, S., Baghian, A. & Kousoulas, K. G. Herpes simplex virus type 1 glycoprotein K is not essential for infectious virus production in actively replicating cells but is required for efficient envelopment and translocation of infectious virions from the cytoplasm to the extracellular space. J. Virol. 71, 5012-5024 (1997). (Pubitemid 27258171)
76. Hutchinson, L, Roop-Beauchamp, C. & Johnson, D. C. Herpes simplex virus glycoprotein K is known to influence fusion of infected cells, yet is not on the cell surface. J. Virol. 69, 4556-4563 (1995).
77. Loret, S., Guay, G. & Lippe, R. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J. Virol. 82, 8605-8618 (2008).
78. Chouljenko, V. N., Iyer, A. V, Chowdhury, S., Kim, J. & Kousoulas, K. G. The herpes simplex virus type-1 (HSV-1) UL20 protein and the amino terminus of glycoprotein K (gK) physically interact with glycoprotein B (gB). J. Virol. 84, 8596-8606 (2010).
79. Mossman, K. L, Sherburne, R., Lavery, C, Duncan, J. & Smiley, J. R. Evidence that herpes simplex virus VP16 is required for viral egress downstream of the initial envelopment event. J. Virol. 74, 6287-6299 (2000). (Pubitemid 30429793)
80. Nozawa, N. et al. Herpes simplex virus type 1 UL51 protein is involved in maturation and egress of virus particles. J. Virol. 79, 6947-6956 (2005). (Pubitemid 40677326)
81. Varnum, S. M. et al. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78, 10960-10966 (2004). (Pubitemid 39299636)
82. Chen, D. H., Jiang, H., Lee, M., Liu, F. & Zhou, Z. H. Three-dimensional visualization of tegument/capsid interactions in the intact human cytomegalovirus. Virology 260, 10-16 (1999). (Pubitemid 29391728)
83. Zhou, Z. H., Chen, D. H., Jakana, J., Rixon, F J. & Chiu, W. Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J. Virol. 73, 3210-3218 (1999). (Pubitemid 29135713)
84. McNabb, D. S. & Courtney, R. J. Characterization of the large tegument protein (ICP1/2) of herpes simplex virus type 1. Virology 190, 221-232 (1992).
85. Schmitz, J. B., Albright, A. G., Kinchington, P. R. & Jenkins, F. J. The UL37 protein of herpes simplex virus type 1 is associated with the tegument of purified virions. Virology 206, 1055-1065 (1995).
86. Newcomb, W. W. & Brown, J. C. Structure and capsid association of the herpesvirus large tegument protein UL36. J. Virol. 84, 9408-9414 (2010).
87. Luxton, G. W., Lee, J. I., Haverlock-Moyns, S., Schober, J. M. & Smith, G. A. The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J. Virol. 80, 201-209 (2006).
88. Coller, K. E., Lee, J. I., Ueda, A. & Smith, G. A. The capsid and tegument of the alpha herpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J. Virol. 81, 11790-11797 (2007). (Pubitemid 47623811)
89. Desai, P., Sexton, G. L., Huang, E. & Person, S. Localization of herpes simplex virus type 1 UL37 in the Golgi complex requires UL36 but not capsid structures. J. Virol. 82, 11354-11361 (2008).
90. Brignati, M. J., Loomis, J. S., Wills, J. W. & Courtney R. J. Membrane association of VP22, a herpes simplex virus type 1 tegument protein. J. Virol. 77, 4888-4898 (2003). (Pubitemid 36402838)
91. Loomis, J. S., Bowzard, J. B., Courtney, R. J. & Wills, J. W. Intracellular trafficking of the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 75, 12209-12219 (2001). (Pubitemid 33115894)
92. Elliott, G., Hafezi, W., Whiteley, A. & Bernard, E. Deletion of the herpes simplex virus VP22-encoding gene (UL49) alters the expression, localization, and virion incorporation of ICP0. J. Virol. 79, 9735-9745 (2005). (Pubitemid 41022316)
93. Duffy, C. et al. Characterization of a UL49-null mutant: VP22 of herpes simplex virus type 1 facilitates viral spread in cultured cells and the mouse cornea. J. Virol. 80, 8664-8675 (2006). (Pubitemid 44384876)
94. Stylianou, J., Maringer, K., Cook, R., Bernard, E. & Elliott, G. Virion incorporation of the herpes simplex virus type 1 tegument protein VP22 occurs via glycoprotein E-specific recruitment to the late secretory pathway. J. Virol. 83, 5204-5218 (2009).
95. Murphy, M. A., Bucks, M. A., O'Regan, K. J. & Courtney, R. J. The HSV 1 tegument protein pUL46 associates with cellular membranes and viral capsids. Virology 376, 279-289 (2008).
96. Elliott, G., Mouzakitis, G. & O'Hare, P. VP16 interacts via its activation domain with VP22, a tegument protein of herpes simplex virus, and is relocated to a novel macromolecular assembly in coexpressing cells. J. Virol. 69, 7932-7941 (1995).
97. Smibert, C. A., Popova, B., Xiao, P., Capone, J. P. & Smiley, J. R. Herpes simplex virus VP16 forms a complex with the virion host shutoff protein vhs. J. Virol. 68, 2339-2346 (1994). (Pubitemid 24091912)
98. Read, G. S., Karr, B. M. & Knight, K. Isolation of a herpes simplex virus type 1 mutant with a deletion in the virion host shutoff gene and identification of multiple forms of the vhs (UL41) polypeptide. J. Virol. 67, 7149-7160 (1993). (Pubitemid 23343841)
99. Lam, Q. et al. Herpes simplex virus VP16 rescues viral mRNA from destruction by the virion host shutoff function. EMBO J. 15, 2575-2581 (1996). (Pubitemid 26151197)
100. Taddeo, B., Sciortino, M. T., Zhang, W. & Roizman, B. Interaction of herpes simplex virus RNase with VP16 and VP22 is required for the accumulation of the protein but not for accumulation of mRNA. Proc. Natl Acad. Sci. USA 104, 12163-12168 (2007). (Pubitemid 47185647)
101. MacLean, C. A., Dolan, A., Jamieson, F E. & McGeoch, D. J. The myristylated virion proteins of herpes simplex virus type 1: investigation of their role in the virus life cycle. J. Gen. Virol. 73, 539-547 (1992).
102. Baines, J. D. & Roizman, B. The UL1 1 gene of herpes simplex virus 1 encodes a function that facilitates nucleocapsid envelopment and egress from cells. J. Virol. 66, 5168-5174 (1992).
103. Kopp, M. et al. The pseudorabies virus UL1 1 protein is a virion component involved in secondary envelopment in the cytoplasm. J. Virol. 77, 5339-5351 (2003). (Pubitemid 36460948)
104. Silva, M. C, Yu, Q. C, Enquist, L. & Shenk, T. Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument-associated capsids. J. Virol. 77, 10594-10605 (2003). (Pubitemid 37129703)
105. Loomis, J. S., Courtney, R. J. & Wills, J. W. Binding partners for the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 77, 11417-11424 (2003). (Pubitemid 37271640)
106. Meckes, D. G. Jr & Wills, J. W. Dynamic interactions of the UL16 tegument protein with the capsid of herpes simplex virus. J. Virol. 81, 13028-13036 (2007). (Pubitemid 350156941)
107. Klupp, B. G., Bottcher, S., Granzow, H., Kopp, M. & Mettenleiter, T. C. Complex formation between the UL16 and UL21 tegument proteins of pseudorabies virus. J. Virol. 79, 1510-1522 (2005). (Pubitemid 40459098)
108. Harper, A. L. et al. Interaction domains of the UL16 and UL21 tegument proteins of herpes simplex virus. J. Virol. 84, 2963-2971 (2010).
109. Meckes, D. G. Jr, Marsh, J. A. & Wills, J. W. Complex mechanisms for the packaging of the UL16 tegument protein into herpes simplex virus. Virology 398, 208-213 (2010).
110. Zhu, Z. et al. Envelopment of varicella-zoster virus: targeting of viral glycoproteins to the trans-Golgi network. J. Virol. 69, 7951-7959 (1995). (Pubitemid 3004483)
111. McMillan, T. N. & Johnson, D. C. Cytoplasmic domain of herpes simplex virus gE causes accumulation in the trans-Golgi network, a site of virus envelopment and sorting of virions to cell junctions. J. Virol. 75, 1928-1940 (2001). (Pubitemid 32110183)
112. Wisner, T. W. & Johnson, D. C. Redistribution of cellular and herpes simplex virus proteins from the trans-Golgi network to cell junctions without enveloped capsids. J. Virol. 78, 11519-11535 (2004). (Pubitemid 39390738)
113. Sanchez, V, Greis, K. D., Sztul, E. & Britt, W. J. Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J. Virol. 74, 75-986 (2000).
114. Harley, C. A., Dasgupta, A. & Wilson, D. W Characterization of herpes simplex virus-containing organelles by subcellular fractionation: role for organelle acidification in assembly of infectious particles. J. Virol. 75, 1236-1251 (2001). (Pubitemid 32094683)
115. Turcotte, S., Letellier, J. & Lippe, R. Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J. Virol. 79, 8847-8860 (2005). (Pubitemid 40934795)
116. Sugimoto, K. et al. Simultaneous tracking of capsid, tegument, and envelope protein localization in living cells infected with triply fluorescent herpes simplex virus 1. J. Virol. 82, 5198-5211 (2008). (Pubitemid 351705229)
117. Campadelli, G. et al. Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc. Natl Acad. Sci. USA 90, 2798-2802 (1993). (Pubitemid 23113504)
118. Gu, F, Crump, C. M. & Thomas, G. Trans-Golgi network sorting. Cell. Mol. Life Sci. 58, 1067-1084 (2001). (Pubitemid 32756518)
119. Beitia Ortiz de Zarate, I., Kaelin, K. & Rozenberg, F Effects of mutations in the cytoplasmic domain of herpes simplex virus type 1 glycoprotein B on intracellular transport and infectivity. J. Virol. 78, 1540-1551 (2004). (Pubitemid 38095863)
120. Crump, C. M., Hung., C. H., Thomas, L, Wan, L. & Thomas, G. Role of PACS-1 in trafficking of human cytomegalovirus glycoprotein B and virus production. J. Virol. 77, 11105-11113 (2003). (Pubitemid 37204300)
121. Zhu, Z., Hao, Y., Gershon, M. D., Ambron, R. T. & Gershon, A. A. Targeting of glycoprotein I (gE) of varicella-zoster virus to the trans-Golgi network by an AYRV sequence and an acidic amino acid-rich patch in the cytosolic domain of the molecule. J. Virol. 70, 6563-6575 (1996). (Pubitemid 26307361)
122. Crump, C. M. et al. Alphaherpesvirus glycoprotein M causes the relocalization of plasma membrane proteins. J. Gen. Virol. 85, 3517-3527 (2004). (Pubitemid 39591859)
123. Farnsworth, A., Goldsmith, K. & Johnson, D. C. Herpes simplex virus glycoproteins gD and gE/gI serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm. J. Virol. 77, 8481-8494 (2003). (Pubitemid 36871476)
124. Brack, A. R. et al. Role of the cytoplasmic tail of pseudorabies virus glycoprotein E in virion formation. J. Virol. 74, 4004-4016 (2000). (Pubitemid 30214405)
125. O'Regan, K. J., Murphy, M. A., Bucks, M. A., Wills, J. W. & Courtney, R. J. Incorporation of the herpes simplex virus type 1 tegument protein VP22 into the virus particle is independent of interaction with VP16. Virology 369, 263-280 (2007). (Pubitemid 350087185)
126. Farnsworth, A., Wisner, T. W. & Johnson, D. C. Cytoplasmic residues of herpes simplex virus glycoprotein gE required for secondary envelopment and binding of tegument proteins VP22 and UL11 to gE and gD. J. Virol. 81, 319-331 (2007). (Pubitemid 44975172)
127. McLauchlan, J. & Rixon, F J. Characterization of enveloped tegument structures (L particles) produced by alphaherpesviruses: integrity of the tegument does not depend on the presence of capsid or envelope. J. Gen. Virol. 73, 269-276 (1992).
128. Irmiere, A. & Gibson, W. Isolation and characterization of a noninfectious virion-like particle released from cells infected with human strains of cytomegalovirus. Virology 130, 118-133 (1983). (Pubitemid 14226847)
129. Pawliczek, T. & Crump, C. M. Herpes simplex virus type 1 production requires a functional ESCRT-III complex but is independent of TSG101 and ALIX expression. J Virol. 83, 11254-11264 (2009).
130. Tandon, R., AuCoin, D. P. & Mocarski, E. S. Human cytomegalovirus exploits ESCRT machinery in the process of virion maturation. J. Virol. 83, 10797-10807 (2009).
131. Roberts, K. L. & Baines, J. D. Myosin Va enhances secretion of herpes simplex virus 1 virions and cell surface expression of viral glycoproteins. J. Virol. 84, 9889-9896 (2010).
132. Johnson, D. C, Webb, M., Wisner, T. W. & Brunetti, C. Herpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread. J. Virol. 75, 821-833 (2001). (Pubitemid 32037284)
133. Polcicova, K. et al. Herpes keratitis in the absence of anterograde transport of virus from sensory ganglia to the cornea. Proc. Natl Acad. Sci. USA 102, 11462-11467 (2005). (Pubitemid 41153842)
134. Corey, L. & Spear, P. G. Infections with herpes simplex viruses (1). N. Engl. J. Med. 314, 686-691 (1986).
135. Penfold, M. E., Armati, P. & Cunningham, A. L. Axonal transport of herpes simplex virions to epidermal cells: evidence for a specialized mode of virus transport and assembly. Proc. Natl Acad. Sci. USA 91, 6529-6533 (1994). (Pubitemid 24200695)
136. Snyder, A., Wisner, T. W. & Johnson, D. C. Herpes simplex virus capsids are transported in neuronal axons without an envelope containing the viral glycoproteins. J. Virol. 80, 11165-11177 (2006). (Pubitemid 44706556)
137. Snyder, A., Bruun, B., Browne, H. M. & Johnson, D. C. A herpes simplex virus gD-YFP fusion glycoprotein is transported separately from viral capsids in neuronal axons. J. Virol. 81, 8337-8340 (2007). (Pubitemid 47101518)
138. Miranda-Saksena, M. et al. Herpes simplex virus utilizes the large secretory vesicle pathway for anterograde transport of tegument and envelope proteins and for viral exocytosis from growth cones of human fetal axons. J. Virol. 83, 3187-3199 (2009).
139. Antinone, S. E. & Smith, G. A. Two modes of herpesvirus trafficking in neurons: membrane acquisition directs motion. J. Virol. 80, 11235-11240 (2006). (Pubitemid 44706563)
140. Maresch, C. et al. Ultrastructural analysis of virion formation and anterograde intraaxonal transport of the alphaherpesvirus pseudorabies virus in primary neurons. J. Virol. 84, 5528-5539 (2010).
141. Antinone, S. E. & Smith, G. A. Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J. Virol. 84, 1504-1512 (2010).
142. Negatsch, A. et al. Ultrastructural analysis of virion formation and intraaxonal transport of herpes simplex virus type 1 in primary rat neurons. J. Virol. 84, 13031-13035 (2010).
143. Ch'ng, T. H. & Enquist, L. W. Efficient axonal localization of alphaherpesvirus structural proteins in cultured sympathetic neurons requires viral glycoprotein E. J. Virol. 79, 8835-8846 (2005). (Pubitemid 40934794)
144. Snyder, A., Polcicova, K. & Johnson, D. C. Herpes simplex virus gE/gI and US9 proteins promote transport of both capsids and virion glycoproteins in neuronal axons. J. Virol. 82, 10613-10624 (2008). (Pubitemid 352691178)
145. Lyman, M. G., Feierbach, B., Curanovic, D., Bisher, M. & Enquist, L. W. PRV Us9 directs axonal sorting of viral capsids. J. Virol. 8 Aug 2007 (doi:10.1128/JVI.01281-07).
146. Enquist, L. W., Tomishima, M. J., Gross, S. & Smith, G. A. Directional spread of an α-herpesvirus in the nervous system. Vet. Microbiol. 86, 5-16 (2002). (Pubitemid 34219144)
147. Johnson, D. C, Wisner, T. W. & Wright, C. C. Herpes simplex virus gB and gD function in a redundant fashion to promote secondary envelopment. J. Virol. 16 Mar 2011 (doi:10.1128/JVI.00011-11).
148. Wisner, T. W., Sugimoto, K., Howard, P. W., Kawaguchi, Y. & Johnson, D. C. Anterograde transport of herpes simplex virus capsids in neurons by both Seperate and Married mechanisms. J. Virol. 30 Mar 2011 (doi:10.1128/JVI.00116- 11)
149. Mooney, R. A., Artsimovitch, I. & Landick, R. Information processing
150. Grachev, M. A. et al. Oligonucleotides complementary to a promoter over the region-8+2 as transcription primers for E. coli RNA polymerase. Nucleic Acids Res. 12, 8509-8524 (1984).
151. Yin, H. et al. Transcription against an applied force. Science 270, 1653-1657 (1995). (Pubitemid 26002439)
152. Ring, B. Z., Yarnell, W. S. & Roberts, J. W. Function of E. coli RNA polymerase s factor s 70 in promoter-proximal pausing. Cell 86, 485-493 (1996). (Pubitemid 26272088)
153. Artsimovitch, I. & Landick, R. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109, 193-203 (2002). (Pubitemid 34518258)
154. Landick, R., Carey, J. & Yanofsky, C. Translation activates the paused transcription complex and restores transcription of the trp operon leader region. Proc. Natl Acad. Sci. USA 82, 4663-4667 (1985). (Pubitemid 16239623)
155. Komissarova, N. & Kashlev, M. RNA polymerase switches between inactivated and activated states by translocating back and forth along the DNA and the RNA. J. Biol. Chem. 272, 15329-15338 (1997). (Pubitemid 27255555)
156. Toulme, F, Mosrin-Huaman, C, Artsimovitch, I. & Rahmouni, A. R. Transcriptional pausing in vivo: a nascent RNA hairpin restricts lateral movements of RNA polymerase in both forward and reverse directions. J. Mol. Biol. 351, 39-51 (2005). (Pubitemid 40967054)
157. Cramer, P. Multisubunit RNA polymerases. Curr. Opin. Struct. Biol. 12, 89-97 (2002). (Pubitemid 34142726)
158. Schmidt, M. C. & Chamberlin, M. J. NusA protein of Escherichia coli is an efficient transcription termination factor for certain terminator sites. J. Mol. Biol. 195, 809-818 (1987).
159. Gusarov, I. & Nudler, E. The mechanism of intrinsic transcription termination. Mol. Cell 3, 495-504 (1999). (Pubitemid 29292606)
160. Toulokhonov, I., Artsimovitch, I. & Landick, R. Allosteric control of RNA polymerase by a site that contacts nascent RNA hairpins. Science 292, 730-733 (2001). (Pubitemid 32385544)
161. Artsimovitch, I. & Landick, R. Interaction of a nascent RNA structure with RNA polymerase is required for hairpin-dependent transcriptional pausing but not for transcript release. Genes Dev. 12, 3110-3122 (1998). (Pubitemid 28469311)
162. Yarnell, W. S. & Roberts, J. W. Mechanism of intrinsic transcription termination and antitermination. Science 284, 611-615 (1999). (Pubitemid 29289580)
163. Santangelo, T. J. & Roberts, J. W. Forward translocation is the natural pathway of RNA release at an intrinsic terminator. Mol. Cell 14, 117-126 (2004). (Pubitemid 38469914)
164. Shankar, S., Hatoum, A. & Roberts, J. W. A transcription antiterminator constructs a NusA-dependent shield to the emerging transcript. Mol. Cell 27, 914-927 (2007). (Pubitemid 47488186)
165. Peters, J. M. et al. Rho directs widespread termination of intragenic and stable RNA transcription. Proc. Natl Acad. Sci. USA 106, 15406-15411 (2009).
166. Sevostyanova, A. & Artsimovitch, I. Functional analysis of Thermus thermophilus transcription factor NusG. Nucleic Acids Res.38, 7432-7445 (2010).
167. Santangelo, T. J., Cubonova, L., Skinner, K. M. & Reeve, J. N. Archaeal intrinsic transcription termination in vivo. J. Bacteriol. 191, 7102-7108 (2009).
168. Roberts, J. W. Termination factor for RNA synthesis. Nature 224, 1168-1174 (1969).
169. Richardson, J. P., Grimley, C. & Lowery, C. Transcription termination factor Rho activity is altered in Escherichia coli with suA gene mutations. Proc. Natl Acad. Sci. USA 72, 1725-1728 (1975).
170. Cardinale, C. J. et al. Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 320, 935-938 (2008). (Pubitemid 351929589)
171. Harinarayanan, R. & Gowrishankar, J. Host factor titration by chromosomal R-loops as a mechanism for runaway plasmid replication in transcription termination-defective mutants of Escherichia coli. J. Mol. Biol. 332, 31-46 (2003). (Pubitemid 36999729)
172. Klumpp, S. & Hwa, T. Stochasticity and traffic jams in the transcription of ribosomal RNA: intriguing role of termination and antitermination. Proc. Natl Acad. Sci. USA 105, 18159-18164 (2008).
173. Washburn, R. S. & Gottesman, M. E. Transcription termination maintains chromosome integrity. Proc. Natl Acad. Sci. USA 108, 792-797 (2011).
174. Richardson, J. & Greenblatt, J. in Escherichia coli and Salmonella Vol. 1 (eds FC. Neidhardt et al.) 822-848 (ASM Press, Washington DC,1996).
175. Ciampi, M. S. Rho-dependent terminators and transcription termination. Microbiology 152, 2515-2528 (2006). (Pubitemid 44405077)
176. Epshtein, V., Dutta, D., Wade, J. & Nudler, E. An allosteric mechanism of Rho-dependent transcription termination. Nature 463, 245-249 (2010).
177. Mooney, R. A. et al. Regulator trafficking on bacterial transcription units in vivo. Mol. Cell 33, 97-108 (2009).
178. R. J. Biol. Chem. 259, 8664-8671 (1984). (Pubitemid 14090633)
179. Gutierrez, P. et al. Solution structure of YaeO, a Rho-specific inhibitor of transcription termination. J. Biol. Chem. 282, 23348-23353 (2007). (Pubitemid 47311918)
180. Pani, B. et al. Mechanism of inhibition of Rho-dependent transcription termination by bacteriophage P4 protein Psu. J. Biol. Chem. 281, 26491-26500 (2006). (Pubitemid 44401858)
181. Weisberg, R. A. & Gottesman, M. E. Processive antitermination. J. Bacteriol. 181, 359-367 (1999). (Pubitemid 29045123)
182. Stewart, V., Landick, R. & Yanofsky, C. Rho-dependent transcription termination in the tryptophanase operon leader region of Escherichia coli K-12. J. Bacteriol. 166, 217-223 (1986). (Pubitemid 16043303)
183. Henkin, T M. Riboswitch RNAs: using RNA to sense cellular metabolism. Genes Dev. 22, 3383-3390 (2008).
184. Merino, E. & Yanofsky, C. Transcription attenuation: a highly conserved regulatory strategy used by bacteria. Trends Genet. 21, 260-264 (2005). (Pubitemid 40558929)
185. Smith, A. M., Fuchs, R. T., Grundy, F J. & Henkin, T M. Riboswitch RNAs: regulation of gene expression by direct monitoring of a physiological signal. RNA Biol. 7, 104-110 (2010).
186. Amster-Choder, O. The bgl sensory system: a transmembrane signaling pathway controlling transcriptional antitermination. Curr. Opin. Microbiol. 8, 127-134 (2005). (Pubitemid 40417952)
187. Phadtare, S. & Severinov, K. RNA remodeling and gene regulation by cold shock proteins. RNA Biol. 7, 788-795 (2010).
188. 2+ ion and histidine ligand. Nature 434, 183-191 (2005). (Pubitemid 40388043)
189. Schmalisch, M. H., Bachem, S. & Stulke, J. Control of the Bacillus subtilis antiterminator protein GlcT by phosphorylation. Elucidation of the phosphorylation chain leading to inactivation of GlcT J. Biol. Chem. 278, 51108-51115 (2003). (Pubitemid 38020346)
190. Demene, H. et al. Structural mechanism of signal transduction between the RNA-binding domain and the phosphotransferase system regulation domain of the LicT antiterminator. J. Biol. Chem. 283, 30838-30849 (2008).
191. Gopinath, S. C. et al. Insights into anti-termination regulation of the hut operon in Bacillus subtilis: importance of the dual RNA-binding surfaces of HutP. Nucleic Acids Res. 36, 3463-3473 (2008). (Pubitemid 351859013)
192. van Tilbeurgh, H. & Declerck, N. Structural insights into the regulation of bacterial signalling proteins containing PRDs. Curr. Opin. Struct. Biol. 11, 685-693 (2001). (Pubitemid 34076629)
193. Raveh, H., Lopian, L., Nussbaum-Shochat, A., Wright, A. & Amster-Choder, O. Modulation of transcription antitermination in the bgl operon of Escherichia coli by the PTS. Proc. Natl Acad. Sci. USA 106, 13523-13528 (2009).
194. Galperin, M. Y Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J. Bacteriol. 188, 4169-4182 (2006). (Pubitemid 43865736)
195. Fox, K. A. et al. Multiple posttranscriptional regulatory mechanisms partner to control ethanolamine utilization in Enterococcus faecalis. Proc. Natl Acad. Sci. USA 106, 4435-4440 (2009).
196. Chai, W. & Stewart, V. RNA sequence requirements for NasR-mediated, nitrate-responsive transcription antitermination of the Klebsiella oxytoca M5al nasF operon leader. J. Mol. Biol. 292, 203-216 (1999). (Pubitemid 29435760)
197. Yanofsky, C. Attenuation in the control of expression of bacterial operons. Nature 289, 751-758 (1981). (Pubitemid 11150411)
198. Gong, F & Yanofsky, C. Analysis of tryptophanase operon expression in vitro: accumulation of TnaC-peptidyl-tRNA in a release factor 2-depleted S-30 extract prevents Rho factor action, simulating induction. J. Biol. Chem. 277, 17095-17100 (2002). (Pubitemid 34967740)
199. Gong, M., Cruz-Vera, L. R. & Yanofsky, C. Ribosome recycling factor and release factor 3 action promotes TnaC-peptidyl-tRNA dropoff and relieves ribosome stalling during tryptophan induction of tna operon expression in Escherichia coli. J. Bacteriol. 189, 3147-3155 (2007). (Pubitemid 46697405)
200. Grundy, F J., Winkler, W. C. & Henkin, T. M. tRNA-mediated transcription antitermination in vitro: codon-anticodon pairing independent of the ribosome. Proc. Natl Acad. Sci. USA 99, 11121-11126 (2002). (Pubitemid 34920889)
201. Grundy, F J. & Henkin, T. M. tRNA as a positive regulator of transcription antitermination in B. subtilis. Cell 74, 475-482 (1993). (Pubitemid 23244613)
202. Green, N. J., Grundy, F J. & Henkin, T. M. The T box mechanism: tRNA as a regulatory molecule. FEBS Lett. 584, 318-324 (2010).
203. Murray, K. D. & Bremer, H. Control of SpoT-dependent ppGpp synthesis and degradation in Escherichia coli. J. Mol. Biol. 259, 41-57 (1996). (Pubitemid 26162620)
204. Winkler, W. C, Cohen-Chalamish, S. & Breaker, R. R. An mRNA structure that controls gene expression by binding FMN. Proc. Natl Acad. Sci. USA 99, 15908-15913 (2002). (Pubitemid 35462722)
205. Park, S. Y, Cromie, M. J., Lee, E. J. & Groisman, E. A. A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 142, 737-748 (2010).
206. Montange, R. K. & Batey, R. T. Riboswitches: emerging themes in RNA structure and function. Annu. Rev. Biophys. 37, 117-133 (2008).
207. Epshtein, V., Mironov, A. S. & Nudler, E. The riboswitch-mediated control of sulfur metabolism in bacteria. Proc. Natl Acad. Sci. USA 100, 5052-5056 (2003). (Pubitemid 36542656)
208. McDaniel, B. A., Grundy, F J., Artsimovitch, I. & Henkin, T. M. Transcription termination control of the 5 box system: direct measurement of S-adenosylmethionine by the leader RNA. Proc. Natl Acad. Sci. USA 100, 3083-3088 (2003). (Pubitemid 36356543)
209. Winkler, W. C, Nahvi, A., Sudarsan, N., Barrick, J. E. & Breaker, R. R. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nature Struct. Biol. 10, 701-707 (2003). (Pubitemid 37052407)
210. Mandal, M. & Breaker, R. R. Adenine riboswitches and gene activation by disruption of a transcription terminator. Nature Struct. Mol. Biol. 11, 29-35 (2004). (Pubitemid 38173438)
211. French, S. L., Santangelo, T. J., Beyer, A. L. & Reeve, J. N. Transcription and translation are coupled in Archaea. Mol. Biol. Evol. 24, 893-895 (2007). (Pubitemid 46536700)
212. Miller, O. L. Jr, Hamkalo, B. A. & Thomas, C. A. Jr Visualization of bacterial genes in action. Science 169, 392-395 (1970).
213. Santangelo, T. J. et al. Polarity in archaeal operon transcription in Thermococcus kodakaraensis. J. Bacteriol. 190, 2244-2248 (2008). (Pubitemid 351355348)
214. Peters, J. M., Vangeloff, A. D. & Landick, R. Bacterial transcription terminators: the RNA 3′-end chronicles. J. Mol. Biol. 23 Mar 2011 (doi:10.1016/j. jmb.2011.03.036)
215. Burns, C. M. & Richardson, J. P. NusG is required to overcome a kinetic limitation to Rho function at an intragenic terminator. Proc. Natl Acad. Sci. USA 92, 4738-4742 (1995).
216. Sullivan, S. & Gottesman, M. Requirement for E. coli NusG protein in factor-dependent transcription termination. Cell 68, 989-994 (1992).
217. Burmann, B. M. et al. A NusE:NusG complex links transcription and translation. Science 328, 501-504 (2010).
218. Proshkin, S., Rahmouni, A. R., Mironov, A. & Nudler, E. Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328, 504-508 (2010).
219. Torres, M., Condon, C, Balada, J. M., Squires, C. & Squires, C. L. Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non-ribosomal and ribosomal RNA antitermination. EMBO J. 20, 3811-3820 (2001). (Pubitemid 32691792)
220. Campbell, A. Comparative molecular biology of lambdoid phages. Annu. Rev. Microbiol. 48, 193-222 (1994). (Pubitemid 24334096)
221. Artsimovitch, I. & Landick, R. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc. Natl Acad. Sci. USA 97, 7090-7095 (2000). (Pubitemid 30431422)
222. Toulokhonov, I., Zhang, J., Palangat, M. & Landick, R. A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing. Mol. Cell 27, 406-419 (2007). (Pubitemid 47126936)
223. Barik, S., Ghosh, B., Whalen, W., Lazinski, D. & Das, A. An antitermination protein engages the elongating transcription apparatus at a promoter-proximal recognition site. Cell 50, 885-899 (1987).
224. Mogridge, J., Mah, T. & Greenblatt, J. A protein-RNA interaction network facilitates the template-independent cooperative assembly on RNA polymerase of a stable antitermination complex containing the lambda N protein. Genes Dev 9, 2831-2845 (1995).
225. Rees, W. A., Weitzel, S. E., Das, A. & von Hippel, P. H. Regulation of the elongation-termination decision at intrinsic terminators by antitermination protein N of phage a;. J. Mol. Biol. 273, 797-813 (1997). (Pubitemid 27493720)
226. Gusarov, I. & Nudler, E. Control of intrinsic transcription termination by N and NusA: the basic mechanisms. Cell 107, 437-449 (2001). (Pubitemid 33152780)
227. Vieu, E. & Rahmouni, A. R. Dual role of boxB RNA motif in the mechanisms of termination/antitermination at the lambda tR1 terminator revealed in vivo. J. Mol. Biol. 339, 1077-1087 (2004). (Pubitemid 39303250)
228. 70 subunit of RNA polymerase is contacted by the a; Q antiterminator during early elongation. Mol. Cell 10, 611-622 (2002). (Pubitemid 35284177)
229. Roberts, J. W. et al. Antitermination by bacteriophage a; Q protein. Cold Spring Harb. Symp. Quant. Biol. 63, 319-325 (1998).
230. Deighan, P., Diez, C. M., Leibman, M., Hochschild, A. & Nickels, B. E. The bacteriophage a; Q antiterminator protein contacts the ß-flap domain of RNA polymerase. Proc. Natl Acad. Sci. USA 105, 15305-15310 (2008).
231. Kaczanowska, M. & Ryden-Aulin, M. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev 71, 477-494 (2007). (Pubitemid 47429282)
232. Condon, C, Squires, C. & Squires, C. L. Control of rRNA transcription in Escherichia coli. Microbiol. Rev. 59, 623-645 (1995).
233. Greive, S. J., Lins, A. F. & von Hippel, P. H. Assembly of an RNA-protein complex. Binding of NusB and NusE (S10) proteins to boxA RNA nucleates the formation of the antitermination complex involved in controlling rRNA transcription in Escherichia coli. J. Biol. Chem. 280, 36397-36408 (2005). (Pubitemid 41633914)
234. Sen, R., King, R. A. & Weisberg, R. A. Modification of the properties of elongating RNA polymerase by persistent association with nascent antiterminator RNA. Mol. Cell 7, 993-1001 (2001). (Pubitemid 32525746)
235. King, R. A., Markov, D., Sen, R., Severinov, K. & Weisberg, R. A. A conserved zinc binding domain in the largest subunit of DNA-dependent RNA polymerase modulates intrinsic transcription termination and antitermination but does not stabilize the elongation complex. J. Mol. Biol. 342, 1143-1154 (2004). (Pubitemid 39207893)
236. Komissarova, N. et al. Inhibition of a transcriptional pause by RNA anchoring to RNA polymerase. Mol. Cell 31, 683-694 (2008).
237. Irnov, I. & Winkler, W C. A regulatory RNA required for antitermination of biofilm and capsular polysaccharide operons in Bacillales. Mol. Microbiol. 76, 559-575 (2010).
238. Bailey, M. J., Hughes, C. & Koronakis, V. RfaH and the ops element, components of a novel system controlling bacterial transcription elongation. Mol. Microbiol. 26, 845-851 (1997). (Pubitemid 27507870)
239. Belogurov, G. A., Mooney, R. A., Svetlov, V., Landick, R. & Artsimovitch, I. Functional specialization of transcription elongation factors. EMBO J. 28, 112-122 (2009).
240. Belogurov, G. A. et al. Structural basis for converting a general transcription factor into an operon-specific virulence regulator. Mol. Cell 26, 117-129 (2007). (Pubitemid 46553793)
241. Mooney, R. A., Schweimer, K., Rosch, P., Gottesman, M. & Landick, R. Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J. Mol. Biol. 391, 341-358 (2009).
242. Chalissery, J. et al. Interaction surface of the transcription terminator Rho required to form a complex with the C-terminal domain of the antiterminator NusG. J. Mol. Biol. 405, 49-64 (2011).
243. Sevostyanova, A., Svetlov, V., Vassylyev, D. G. & Artsimovitch, I. The elongation factor RfaH and the initiation factor σ bind to the same site on the transcription elongation complex. Proc. Natl Acad. Sci. USA 105, 865-870 (2008). (Pubitemid 351282047)
244. Svetlov, V., Belogurov, G. A., Shabrova, E., Vassylyev, D. G. & Artsimovitch, I. Allosteric control of the RNA polymerase by the elongation factor RfaH. Nucleic Acids Res. 35, 5694-5705 (2007). (Pubitemid 47506287)
245. Bailey, M. J., Hughes, C. & Koronakis, V. In vitro recruitment of the RfaH regulatory protein into a specialised transcription complex, directed by the nucleic acid ops element. Mol. Gen. Genet. 262, 1052-1059 (2000). (Pubitemid 30072134)
246. Nudler, E., Avetissova, E., Markovtsov, V. & Goldfarb, A. Transcription processivity: protein-DNA interactions holding together the elongation complex. Science 273, 2 11-217 (1996).
247. Sidorenkov, I., Komissarova, N. & Kashlev, M. Crucial role of the RNA:DNA hybrid in the processivity of transcription. Mol. Cell 2, 55-64 (1998). (Pubitemid 128378966)
248. Nudler, E. RNA polymerase active center: the molecular engine of transcription. Ann. Rev Biochem. 78, 335-361 (2009).
249. Epshtein, V., Cardinale, C. J., Ruckenstein, A. E., Borukhov, S. & Nudler, E. An allosteric path to transcription termination. Mol. Cell 28, 991-1001 (2007). (Pubitemid 350297020)
250. Park, J. S. & Roberts, J. W Role of DNA bubble rewinding in enzymatic transcription termination. Proc. Natl Acad. Sci. USA 103, 4870-4875 (2006).
251. Potter, K. D., Merlino, N. M., Jacobs, T. & Gollnick, P. TRAP binding to the Bacillus subtilis trp leader region RNA causes efficient transcription termination at a weak intrinsic terminator. Nucleic Acids Res. 39, 2092-2102 (2011).
252. Komissarova, N., Becker, J., Solter, S., Kireeva, M. & Kashlev, M. Shortening of RNA:DNA hybrid in the elongation complex of RNA polymerase is a prerequisite for transcription termination. Mol. Cell 10, 1151-1162 (2002). (Pubitemid 35453832)
253. Larson, M. H., Greenleaf, W J., Landick, R. & Block, S. M. Applied force reveals mechanistic and energetic details of transcription termination. Cell 132, 971-982 (2008). (Pubitemid 351381740)
254. Datta, K. & von Hippel, P. H. Direct spectroscopic study of reconstituted transcription complexes reveals that intrinsic termination is driven primarily by thermodynamic destabilization of the nucleic acid framework. J. Biol. Chem. 283, 3537-3549 (2008).
255. Ha, K. S., Toulokhonov, I., Vassylyev, D. G. & Landick, R. The NusA N-terminal domain is necessary and sufficient for enhancement of transcriptional pausing via interaction with the RNA exit channel of RNA polymerase. J. Mol. Biol. 401, 708-725 (2010).
256. Yuzenkova, Y., Zenkin, N. & Severinov, K. Mapping of RNA polymerase residues that interact with bacteriophage Xp10 transcription antitermination factor p7. J. Mol. Biol. 375, 29-35 (2008). (Pubitemid 350160702)
257. Sydow, J. F. et al. Structural basis of transcription: mismatch-specific fidelity mechanisms and paused RNA polymerase II with frayed RNA. Mol. Cell 34, 710-721 (2009).
258. Belogurov, G. A., Sevostyanova, A., Svetlov, V. & Artsimovitch, I. Functional regions of the N-terminal domain of the antiterminator RfaH. Mol. Microbiol. 76, 286-301 (2010).
259. Werner, F. & Grohmann, D. Evolution of multisubunit RNA polymerases in the three domains of life. Nature Rev Microbiol. 9, 85-98 (2011).
260. Hirtreiter, A. et al. Spt4/5 stimulates transcription elongation through the RNA polymerase clamp coiled-coil motif. Nucleic Acids Res. 38, 4040-4051 (2010).
261. Klein, B. J. et al. RNA polymerase and transcription elongation factor Spt4/5 complex structure. Proc. Natl Acad. Sci. USA 108, 546-550 (2011).
262. Martinez-Rucobo, F. W, Sainsbury, S., Cheung, A. C. & Cramer, P. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J. 8 Mar 2011 (doi:10.1038/emboj.2011.64).
263. Steinmetz, E. J. & Platt, T Evidence supporting a tethered tracking model for helicase activity of Escherichia coli Rho factor. Proc. Natl Acad. Sci. USA 91, 1401-1405 (1994). (Pubitemid 24059019)
264. Rabhi, M. et al. Mutagenesis-based evidence for an asymmetric configuration of the ring-shaped transcription termination factor Rho. J. Mol. Biol. 405, 497-518 (2011).
265. Thomsen, N. D. & Berger, J. M. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 139, 523-534 (2009).
266. Rees, W, Weitzel, S., Yager, T., Das, A. & von Hippel, P. Bacteriophage a; N protein alone can induce transcription antitermination in vitro. Proc. Natl Acad. Sci. USA 93, 342-346 (1996). (Pubitemid 26038155)
267. Sloan, S., Rutkai, E., King, R. A., Velikodvorskaya, T & Weisberg, R. A. Protection of antiterminator RNA by the transcript elongation complex. Mol. Microbiol. 63, 1197-1208 (2007). (Pubitemid 46184522)