Gene expression profiling of monkeypox virus-infected cells reveals novel interfaces for host-virus interactions

Virology Journal

Volumn 7, Issue , 2010, Pages

  Alkhalil, Abdulnaser ^a   Hammamieh, Rasha ^b   Hardick, Justin ^a   Ichou, Mohamed Ait ^a   Jett, Marti ^b   Ibrahim, Sofi ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^b WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ATM PROTEIN; CLATHRIN; G PROTEIN COUPLED RECEPTOR; HISTONE; HISTONE DEACETYLASE 2; ION CHANNEL; SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CONTROLLED STUDY; COPY NUMBER VARIATION; DOWN REGULATION; EPITHELIUM CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENOME ANALYSIS; HOMEOSTASIS; INHIBITION KINETICS; KIDNEY CELL; KIDNEY EPITHELIUM; MACACA; MEMBRANE POTENTIAL; MICROARRAY ANALYSIS; MITOSIS; MONKEYPOX; MONKEYPOX VIRUS; NONHUMAN; OSMOSIS; PROTEIN FUNCTION; RHESUS MONKEY; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS CELL INTERACTION; VIRUS REPLICATION; ANIMAL; CELL LINE; CERCOPITHECUS; DISEASE MODEL; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; MACACA MULATTA; PHYSIOLOGY; VERO CELL; VIROLOGY;

MACACA MULATTA; MONKEYPOX VIRUS; MOROCCAN PEPPER VIRUS; ORTHOPOXVIRUS;

ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA MULATTA; MONKEYPOX; MONKEYPOX VIRUS; VERO CELLS;

EID: 77954923611     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-7-173     Document Type: Article

References (95)

1. Human monkeypox, 1970-79. JG Breman R Kalisa MV Steniowski E Zanotto AI Gromyko I Arita, Bull World Health Organ 1980 58 165 182 6249508
2. A tale of two clades: monkeypox viruses. AM Likos SA Sammons VA Olson AM Frace Y Li M Olsen-Rasmussen W Davidson R Galloway ML Khristova MG Reynolds, et al. J Gen Virol 2005 86 2661 2672 10.1099/vir.0.81215-0 16186219
3. Virulence differences between monkeypox virus isolates from West Africa and the Congo basin. N Chen G Li MK Liszewski JP Atkinson PB Jahrling Z Feng J Schriewer C Buck C Wang EJ Lefkowitz, et al. Virology 2005 340 46 63 10.1016/j.virol.2005.05.030 16023693
4. Analysis of the monkeypox virus genome. SN Shchelkunov AV Totmenin PF Safronov MV Mikheev VV Gutorov OI Ryazankina NA Petrov IV Babkin EA Uvarova LS Sandakhchiev, et al. Virology 2002 297 172 194 10.1006/viro.2002.1446 12083817
5. Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. GC Carter M Law M Hollinshead GL Smith, J Gen Virol 2005 86 1279 1290 10.1099/vir.0.80831-0 15831938
6. Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. JC Hsiao CS Chung W Chang, J Virol 1999 73 8750 8761 10482629
7. A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. CS Chung JC Hsiao YS Chang W Chang, J Virol 1998 72 1577 1585 9445060
8. Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. CL Lin CS Chung HG Heine W Chang, J Virol 2000 74 3353 3365 10.1128/JVI.74.7.3353-3365.2000 10708453
9. The mode of entry of vaccinia virus into L cells. JA Armstrong DH Metz MR Young, J Gen Virol 1973 21 533 537 10.1099/0022-1317-21-3-533 4128637
10. the cycle of multiplication of vaccinia virus in earle's strain l cells. I. Uptake and penetration. S Dales R Kajioka, Virology 1964 24 278 294 10.1016/0042-6822(64)90167-9 14227031
11. Adsorption and penetration of enveloped and naked vaccinia virus particles. LG Payne E Norrby, J Virol 1978 27 19 27 691111
12. Intracellular and extracellular vaccinia virions enter cells by different mechanisms. A Vanderplasschen M Hollinshead GL Smith, J Gen Virol 1998 79 Pt 4 877 887 9568984
13. RNA polymerase activity in purified infectious vaccinia virus. W Munyon E Paoletti JT Grace Jr, Proc Natl Acad Sci USA 1967 58 2280 2287 10.1073/pnas.58.6.2280 5242206
14. Poxvirus DNA-dependent RNA polymerase. JR Kates BR McAuslan, Proc Natl Acad Sci USA 1967 58 134 141 10.1073/pnas.58.1.134 5231593
15. Poxvirus DNA topoisomerase knockout mutant exhibits decreased infectivity associated with reduced early transcription. F Da Fonseca B Moss, Proc Natl Acad Sci USA 2003 100 11291 11296 10.1073/pnas.1534874100 12972642
16. Poxvirus host range genes. SJ Werden MM Rahman G McFadden, Adv Virus Res 2008 71 135 171 full-text 18585528
17. Poxvirus tropism. G McFadden, Nat Rev Microbiol 2005 3 201 213 10.1038/nrmicro1099 15738948
18. Comparative Analysis of Viral Gene Expression Programs during Poxvirus Infection: A Transcriptional Map of the Vaccinia and Monkeypox Genomes. KH Rubins LE Hensley GW Bell C Wang EJ Lefkowitz PO Brown DA Relman, PLoS ONE 2008 3 2628 10.1371/journal.pone.0002628 18612436
19. Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. E Assarsson JA Greenbaum M Sundstrom L Schaffer JA Hammond V Pasquetto C Oseroff RC Hendrickson EJ Lefkowitz DC Tscharke, et al. Proc Natl Acad Sci USA 2008 105 2140 2145 10.1073/pnas.0711573105 18245380
20. Cellular gene expression survey of vaccinia virus infection of human HeLa cells. S Guerra LA Lopez-Fernandez A Pascual-Montano M Munoz K Harshman M Esteban, J Virol 2003 77 6493 6506 10.1128/JVI.77.11.6493-6506.2003 12743306
21. The host response to smallpox: analysis of the gene expression program in peripheral blood cells in a nonhuman primate model. KH Rubins LE Hensley PB Jahrling AR Whitney TW Geisbert JW Huggins A Owen JW Leduc PO Brown DA Relman, Proc Natl Acad Sci USA 2004 101 15190 15195 10.1073/pnas.0405759101 15477590
22. Microarray analysis of A549 cells infected with rabbitpox virus (RPV): a comparison of wild-type RPV and RPV deleted for the host range gene, SPI-1. LM Brum MC Lopez JC Varela HV Baker RW Moyer, Virology 2003 315 322 334 10.1016/S0042-6822(03)00532-4 14585335
23. Axenic growth and drug sensitivity studies of Balamuthia mandrillaris, an agent of amebic meningoencephalitis in humans and other animals. FL Schuster GS Visvesvara, J Clin Microbiol 1996 34 385 388 8789020
24. Plaque assay of variola virus in a cynomolgus monkey kidney cell line. Y Tsuchiya I Tagaya, Arch Gesamte Virusforsch 1970 32 73 81 10.1007/BF01241522 4321456
25. Inhibition of influenza virus matrix (M1) protein expression and virus replication by U6 promoter-driven and lentivirus-mediated delivery of siRNA. EK Hui EM Yap DS An IS Chen DP Nayak, J Gen Virol 2004 85 1877 1884 10.1099/vir.0.79906-0 15218172
26. Expression monitoring by hybridization to high-density oligonucleotide arrays. DJ Lockhart H Dong MC Byrne MT Follettie MV Gallo MS Chee M Mittmann C Wang M Kobayashi H Horton EL Brown, Nat Biotechnol 1996 14 1675 1680 10.1038/nbt1296-1675 9634850
27. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. SN Willis L Chen G Dewson A Wei E Naik JI Fletcher JM Adams DC Huang, Genes Dev 2005 19 1294 1305 10.1101/gad.1304105 15901672
28. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. E Oda R Ohki H Murasawa J Nemoto T Shibue T Yamashita T Tokino T Taniguchi N Tanaka, Science 2000 288 1053 1058 10.1126/science.288. 5468.1053 10807576
29. Synergistic induction of apoptosis by p53-inducible Bcl-2 family proteins Noxa and Puma. W Nakajima N Tanaka, J Nippon Med Sch 2007 74 148 157 10.1272/jnms.74.148 17507791
30. Chemotherapy: targeting the mitochondrial cell death pathway. KM Debatin D Poncet G Kroemer, Oncogene 2002 21 8786 8803 10.1038/sj.onc.1206039 12483532
31. A novel, high conductance channel of mitochondria linked to apoptosis in mammalian cells and Bax expression in yeast. EV Pavlov M Priault D Pietkiewicz EH Cheng B Antonsson S Manon SJ Korsmeyer CA Mannella KW Kinnally, J Cell Biol 2001 155 725 731 10.1083/jcb.200107057 11724814
32. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. S Shimizu A Konishi T Kodama Y Tsujimoto, Proc Natl Acad Sci USA 2000 97 3100 3105 10.1073/pnas.97.7.3100 10737788
33. Caspases induce cytochrome c release from mitochondria by activating cytosolic factors. E Bossy-Wetzel DR Green, J Biol Chem 1999 274 17484 17490 10.1074/jbc.274.25.17484 10364179
34. Inhibition of integrin-mediated crosstalk with epidermal growth factor receptor/Erk or Src signaling pathways in autophagic prostate epithelial cells induces caspase-independent death. MJ Edick L Tesfay LE Lamb BS Knudsen CK Miranti, Mol Biol Cell 2007 18 2481 2490 10.1091/mbc.E06-04-0261 17475774
35. p73 Induces apoptosis via PUMA transactivation and Bax mitochondrial translocation. G Melino F Bernassola M Ranalli K Yee WX Zong M Corazzari RA Knight DR Green C Thompson KH Vousden, J Biol Chem 2004 279 8076 8083 10.1074/jbc.M307469200 14634023
36. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. WC Earnshaw LM Martins SH Kaufmann, Annu Rev Biochem 1999 68 383 424 10.1146/annurev.biochem.68.1.383 10872455
37. The role of the ubiquitin-proteasome pathway in apoptosis. RZ Orlowski, Cell Death Differ 1999 6 303 313 10.1038/sj.cdd.4400505 10381632
38. Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. N Mailand AV Podtelejnikov A Groth M Mann J Bartek J Lukas, EMBO J 2002 21 5911 5920 10.1093/emboj/cdf567 12411508
39. Cdc25B cooperates with Cdc25A to induce mitosis but has a unique role in activating cyclin B1-Cdk1 at the centrosome. A Lindqvist H Kallstrom A Lundgren E Barsoum CK Rosenthal, J Cell Biol 2005 171 35 45 10.1083/jcb.200503066 16216921
40. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. CY Peng PR Graves RS Thoma Z Wu AS Shaw H Piwnica-Worms, Science 1997 277 1501 1505 10.1126/science.277.5331.1501 9278512
41. Suppression of Neu-induced mammary tumor growth in cyclin D1 deficient mice is compensated for by cyclin E. DB Bowe NJ Kenney Y Adereth IG Maroulakou, Oncogene 2002 21 291 298 10.1038/sj.onc.1205025 11803472
42. The low molecular weight cyclin E isoforms augment angiogenesis and metastasis of human melanoma cells in vivo. E Bales L Mills N Milam M McGahren-Murray D Bandyopadhyay D Chen JA Reed N Timchenko JJ van den Oord M Bar-Eli, et al. Cancer Res 2005 65 692 697 15705861
43. Enhanced tumor formation in cyclin D1 × transforming growth factor beta1 double transgenic mice with characterization by magnetic resonance imaging. NG Deane H Lee J Hamaamen A Ruley MK Washington B LaFleur SS Thorgeirsson R Price RD Beauchamp, Cancer Res 2004 64 1315 1322 10.1158/0008-5472.CAN-03-1772 14973059
44. Eph receptors and ephrins. M Nakamoto, Int J Biochem Cell Biol 2000 32 7 12 10.1016/S1357-2725(99)00096-5 10661890
45. Large-scale mapping of human protein-protein interactions by mass spectrometry. RM Ewing P Chu F Elisma H Li P Taylor S Climie L McBroom-Cerajewski MD Robinson L O'Connor M Li, et al. Mol Syst Biol 2007 3 89 10.1038/msb4100134 17353931
46. Reconstitution of cyclin D1-associated kinase activity drives terminally differentiated cells into the cell cycle. L Latella A Sacco D Pajalunga M Tiainen D Macera M D'Angelo A Felici A Sacchi M Crescenzi, Mol Cell Biol 2001 21 5631 5643 10.1128/MCB.21.16.5631-5643.2001 11463844
47. Cyclin D1 suppresses retinoblastoma protein-mediated inhibition of TAFII250 kinase activity. JL Siegert JJ Rushton WR Sellers WG Kaelin Jr PD Robbins, Oncogene 2000 19 5703 5711 10.1038/sj.onc.1203966 11126356
48. Cell cycle regulation and apoptosis. KL King JA Cidlowski, Annu Rev Physiol 1998 60 601 617 10.1146/annurev.physiol.60.1.601 9558478
49. Disruption of the G1/S transition in human papillomavirus type 16 E7-expressing human cells is associated with altered regulation of cyclin E. LG Martin GW Demers DA Galloway, J Virol 1998 72 975 985 9444990
50. Balancing the decision of cell proliferation and cell fate. TC Hallstrom JR Nevins, Cell Cycle 2009 8 532 535 19182518
51. The INK4 family of cell cycle inhibitors in cancer. MF Roussel, Oncogene 1999 18 5311 5317 10.1038/sj.onc.1202998 10498883
52. Molecular interaction map of the mammalian cell cycle control and DNA repair systems. KW Kohn, Mol Biol Cell 1999 10 2703 2734 10436023
53. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. J Falck N Mailand RG Syljuasen J Bartek J Lukas, Nature 2001 410 842 847 10.1038/35071124 11298456
54. Rapid destruction of human Cdc25A in response to DNA damage. N Mailand J Falck C Lukas RG Syljuasen M Welcker J Bartek J Lukas, Science 2000 288 1425 1429 10.1126/science.288.5470.1425 10827953
55. MAP kinases and CDKs: kinetic basis for catalytic activation. J Lew, Biochemistry 2003 42 849 856 10.1021/bi0269761 12549901
56. CDK inhibitors: positive and negative regulators of G1-phase progression. CJ Sherr JM Roberts, Genes Dev 1999 13 1501 1512 10.1101/gad.13.12.1501 10385618
57. Non-malignant and tumor-derived cells differ in their requirement for p27Kip1 in transforming growth factor-beta-mediated G1 arrest. JC Donovan JM Rothenstein JM Slingerland, J Biol Chem 2002 277 41686 41692 10.1074/jbc.M204307200 12202478
58. Role of glycogen synthase kinase-3 in cancer: regulation by Wnts and other signaling pathways. AS Manoukian JR Woodgett, Adv Cancer Res 2002 84 203 229 full-text 11883528
59. The Janus kinase 2 is required for expression and nuclear accumulation of cyclin D1 in proliferating mammary epithelial cells. K Sakamoto BA Creamer AA Triplett KU Wagner, Mol Endocrinol 2007 21 1877 1892 10.1210/me.2006-0316 17519353
60. Cdc25-dependent activation of cyclin A/cdk2 is blocked in G2 phase arrested cells independently of ATM/ATR. S Goldstone S Pavey A Forrest J Sinnamon B Gabrielli, Oncogene 2001 20 921 932 10.1038/sj.onc.1204177 11314027
61. The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system. A Kumagai WG Dunphy, Cell 1991 64 903 914 10.1016/0092-8674(91)90315-P 1825803
62. The genetic defect in ataxia-telangiectasia. MF Lavin Y Shiloh, Annu Rev Immunol 1997 15 177 202 10.1146/annurev.immunol.15.1.177 9143686
63. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. CE Canman DS Lim KA Cimprich Y Taya K Tamai K Sakaguchi E Appella MB Kastan JD Siliciano, Science 1998 281 1677 1679 10.1126/science.281.5383.1677 9733515
64. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. WA Cliby CJ Roberts KA Cimprich CM Stringer JR Lamb SL Schreiber SH Friend, EMBO J 1998 17 159 169 10.1093/emboj/17.1.159 9427750
65. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. H Zhao H Piwnica-Worms, Mol Cell Biol 2001 21 4129 4139 10.1128/MCB.21.13.4129-4139.2001 11390642
66. Mammalian Polo-like kinase 3 (Plk3) is a multifunctional protein involved in stress response pathways. M Bahassi el CW Conn DL Myer RF Hennigan CH McGowan Y Sanchez PJ Stambrook, Oncogene 2002 21 6633 6640 10.1038/sj.onc. 1205850 12242661
67. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Y Sanchez C Wong RS Thoma R Richman Z Wu H Piwnica-Worms SJ Elledge, Science 1997 277 1497 1501 10.1126/science.277. 5331.1497 9278511
68. The biochemistry of apoptosis. MO Hengartner, Nature 2000 407 770 776 10.1038/35037710 11048727
69. Poxviruses and apoptosis: a time to die. H Everett G McFadden, Curr Opin Microbiol 2002 5 395 402 10.1016/S1369-5274(02)00340-5 12160859
70. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. M Thome P Schneider K Hofmann H Fickenscher E Meinl F Neipel C Mattmann K Burns JL Bodmer M Schroter, et al. Nature 1997 386 517 521 10.1038/386517a0 9087414
71. Ultraviolet-induced cell death blocked by a selenoprotein from a human dermatotropic poxvirus. JL Shisler TG Senkevich MJ Berry B Moss, Science 1998 279 102 105 10.1126/science.279.5347.102 9417017
72. Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. T Komiyama CA Ray DJ Pickup AD Howard NA Thornberry EP Peterson G Salvesen, J Biol Chem 1994 269 19331 19337 8034697
73. Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. LT Quan A Caputo RC Bleackley DJ Pickup GS Salvesen, J Biol Chem 1995 270 10377 10379 10.1074/jbc.270.52.31046 7737968
74. Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. M Dobbelstein T Shenk, J Virol 1996 70 6479 6485 8709286
75. The E3L and K3L vaccinia virus gene products stimulate translation through inhibition of the double-stranded RNA-dependent protein kinase by different mechanisms. MV Davies HW Chang BL Jacobs RJ Kaufman, J Virol 1993 67 1688 1692 8094759
76. Vaccinia virus encodes a previously uncharacterized mitochondrial- associated inhibitor of apoptosis. ST Wasilenko TL Stewart AF Meyers M Barry, Proc Natl Acad Sci USA 2003 100 14345 14350 10.1073/pnas.2235583100 14610284
77. Prevention of immune cell apoptosis as potential therapeutic strategy for severe infections. J Parrino RS Hotchkiss M Bray, Emerg Infect Dis 2007 13 191 198 10.3201/eid1302.060963 17479879
78. The genome of fowlpox virus. CL Afonso ER Tulman Z Lu L Zsak GF Kutish DL Rock, J Virol 2000 74 3815 3831 10.1128/JVI.74.8.3815-3831.2000 10729156
79. Characterization of supercoiled nucleoprotein complexes released from detergent-treated vaccinia virions. MJ Soloski JA Holowczak, J Virol 1981 37 770 783 7218437
80. The osmium ammine-SO2 staining method for studying the in situ configuration of viral genomes in ultrathin sections of DNA virus infected cells. F Puvion-Dutilleul EH Leduc E Puvion, Biol Cell 1996 87 133 141 10.1016/S0248-4900(97)89270-2 9075323
81. Chromatin at the intersection of viral infection and DNA damage. CE Lilley MS Chaurushiya MD Weitzman, Biochim Biophys Acta 2009 1799 319 327 19616655
82. SV40 DNA replication: from the A gene to a nanomachine. E Fanning K Zhao, Virology 2009 384 352 359 10.1016/j.virol.2008.11.038 19101707
83. Rapid microtubule-dependent induction of neurite-like extensions in NIH 3T3 fibroblasts by inhibition of ROCK and Cbl. RM Scaife D Job WY Langdon, Mol Biol Cell 2003 14 4605 4617 10.1091/mbc.E02-11-0739 12960437
84. The N-terminal region of GAP regulates cytoskeletal structure and cell adhesion. J McGlade B Brunkhorst D Anderson G Mbamalu J Settleman S Dedhar M Rozakis-Adcock LB Chen T Pawson, EMBO J 1993 12 3073 3081 8344248
85. Post-transcriptional down-regulation of ROCKI/Rho-kinase through an MEK-dependent pathway leads to cytoskeleton disruption in Ras-transformed fibroblasts. G Pawlak DM Helfman, Mol Biol Cell 2002 13 336 347 10.1091/mbc.01-06-0302 11809843
86. Integrin signaling. FG Giancotti E Ruoslahti, Science 1999 285 1028 1032 10.1126/science.285.5430.1028 10446041
87. Ion channel regulation by Ras, Rho, and Rab small GTPases. O Pochynyuk JD Stockand A Staruschenko, Exp Biol Med (Maywood) 2007 232 1258 1265 10.3181/0703-MR-76 17959838
88. The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. H Everett M Barry X Sun SF Lee C Frantz LG Berthiaume G McFadden RC Bleackley, J Exp Med 2002 196 1127 1139 10.1084/jem.20011247 12417624
89. Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1-infected cells. U Schubert AV Ferrer-Montiel M Oblatt-Montal P Henklein K Strebel M Montal, FEBS Lett 1996 398 12 18 10.1016/S0014-5793(96)01146-5 8946945
90. A voltage-dependent channel involved in nutrient uptake by red blood cells infected with the malaria parasite. SA Desai SM Bezrukov J Zimmerberg, Nature 2000 406 1001 1005 10.1038/35023000 10984055
91. Human immunodeficiency virus type 1 Vpr-mediated G(2) cell cycle arrest: Vpr interferes with cell cycle signaling cascades by interacting with the B subunit of serine/threonine protein phosphatase 2A. M Hrimech XJ Yao PE Branton EA Cohen, EMBO J 2000 19 3956 3967 10.1093/emboj/19.15.3956 10921877
92. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J He S Choe R Walker P Di Marzio DO Morgan NR Landau, J Virol 1995 69 6705 6711 7474080
93. Human immunodeficiency virus type 1 Vpr arrests the cell cycle in G2 by inhibiting the activation of p34cdc2-cyclin B. F Re D Braaten EK Franke J Luban, J Virol 1995 69 6859 6864 7474100
94. Viral infections and cell cycle G2/M regulation. RY Zhao RT Elder, Cell Res 2005 15 143 149 10.1038/sj.cr.7290279 15780175
95. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. V Janssens J Goris, Biochem J 2001 353 417 439 10.1042/0264-6021:3530417 11171037