Mutations in the Basic Region of the Mason-Pfizer Monkey Virus Nucleocapsid Protein Affect Reverse Transcription, Genomic RNA Packaging, and the Virus Assembly Site

. 2018 May 15 ; 92 (10) : . [epub] 20180427

Jazyk angličtina Země Spojené státy americké Médium electronic-print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29491167

In addition to specific RNA-binding zinc finger domains, the retroviral Gag polyprotein contains clusters of basic amino acid residues that are thought to support Gag-viral genomic RNA (gRNA) interactions. One of these clusters is the basic K16NK18EK20 region, located upstream of the first zinc finger of the Mason-Pfizer monkey virus (M-PMV) nucleocapsid (NC) protein. To investigate the role of this basic region in the M-PMV life cycle, we used a combination of in vivo and in vitro methods to study a series of mutants in which the overall charge of this region was more positive (RNRER), more negative (AEAEA), or neutral (AAAAA). The mutations markedly affected gRNA incorporation and the onset of reverse transcription. The introduction of a more negative charge (AEAEA) significantly reduced the incorporation of M-PMV gRNA into nascent particles. Moreover, the assembly of immature particles of the AEAEA Gag mutant was relocated from the perinuclear region to the plasma membrane. In contrast, an enhancement of the basicity of this region of M-PMV NC (RNRER) caused a substantially more efficient incorporation of gRNA, subsequently resulting in an increase in M-PMV RNRER infectivity. Nevertheless, despite the larger amount of gRNA packaged by the RNRER mutant, the onset of reverse transcription was delayed in comparison to that of the wild type. Our data clearly show the requirement for certain positively charged amino acid residues upstream of the first zinc finger for proper gRNA incorporation, assembly of immature particles, and proceeding of reverse transcription.IMPORTANCE We identified a short sequence within the Gag polyprotein that, together with the zinc finger domains and the previously identified RKK motif, contributes to the packaging of genomic RNA (gRNA) of Mason-Pfizer monkey virus (M-PMV). Importantly, in addition to gRNA incorporation, this basic region (KNKEK) at the N terminus of the nucleocapsid protein is crucial for the onset of reverse transcription. Mutations that change the positive charge of the region to a negative one significantly reduced specific gRNA packaging. The assembly of immature particles of this mutant was reoriented from the perinuclear region to the plasma membrane. On the contrary, an enhancement of the basic character of this region increased both the efficiency of gRNA packaging and the infectivity of the virus. However, the onset of reverse transcription was delayed even in this mutant. In summary, the basic region in M-PMV Gag plays a key role in the packaging of genomic RNA and, consequently, in assembly and reverse transcription.

Zobrazit více v PubMed

von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J Virol 77:5439–5450. doi:10.1128/JVI.77.9.5439-5450.2003. PubMed DOI PMC

Zhao G, Perilla JR, Yufenyuy EL, Meng X, Chen B, Ning J, Ahn J, Gronenborn AM, Schulten K, Aiken C, Zhang P. 2013. Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 497:643–646. doi:10.1038/nature12162. PubMed DOI PMC

Pornillos O, Ganser-Pornillos BK, Kelly BN, Hua Y, Whitby FG, Stout CD, Sundquist WI, Hill CP, Yeager M. 2009. X-ray structures of the hexameric building block of the HIV capsid. Cell 137:1282–1292. doi:10.1016/j.cell.2009.04.063. PubMed DOI PMC

Pornillos O, Ganser-Pornillos BK, Yeager M. 2011. Atomic-level modelling of the HIV capsid. Nature 469:424–427. doi:10.1038/nature09640. PubMed DOI PMC

Bharat TA, Davey NE, Ulbrich P, Riches JD, de Marco A, Rumlova M, Sachse C, Ruml T, Briggs JA. 2012. Structure of the immature retroviral capsid at 8 A resolution by cryo-electron microscopy. Nature 487:385–389. doi:10.1038/nature11169. PubMed DOI

Schur FK, Hagen WJ, Rumlova M, Ruml T, Muller B, Krausslich HG, Briggs JA. 2015. Structure of the immature HIV-1 capsid in intact virus particles at 8.8 A resolution. Nature 517:505–508. doi:10.1038/nature13838. PubMed DOI

Zhang Y, Qian H, Love Z, Barklis E. 1998. Analysis of the assembly function of the human immunodeficiency virus type 1 Gag protein nucleocapsid domain. J Virol 72:1782–1789. PubMed PMC

Rein A, Henderson LE, Levin JG. 1998. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem Sci 23:297–301. doi:10.1016/S0968-0004(98)01256-0. PubMed DOI

Gorelick RJ, Nigida SM Jr, Bess JW Jr, Arthur LO, Henderson LE, Rein A. 1990. Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J Virol 64:3207–3211. PubMed PMC

Darlix JL, Gabus C, Nugeyre MT, Clavel F, Barre-Sinoussi F. 1990. cis elements and trans-acting factors involved in the RNA dimerization of the human immunodeficiency virus HIV-1. J Mol Biol 216:689–699. doi:10.1016/0022-2836(90)90392-Y. PubMed DOI

Henderson LE, Copeland TD, Sowder RC, Smythers GW, Oroszlan S. 1981. Primary structure of the low molecular weight nucleic acid-binding proteins of murine leukemia viruses. J Biol Chem 256:8400–8406. PubMed

Aldovini A, Young RA. 1990. Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. J Virol 64:1920–1926. PubMed PMC

Gorelick RJ, Henderson LE, Hanser JP, Rein A. 1988. Point mutants of Moloney murine leukemia virus that fail to package viral RNA: evidence for specific RNA recognition by a “zinc finger-like” protein sequence. Proc Natl Acad Sci U S A 85:8420–8424. doi:10.1073/pnas.85.22.8420. PubMed DOI PMC

Dorfman T, Luban J, Goff SP, Haseltine WA, Gottlinger HG. 1993. Mapping of functionally important residues of a cysteine-histidine box in the human immunodeficiency virus type 1 nucleocapsid protein. J Virol 67:6159–6169. PubMed PMC

Bess JW, Powell PJ, Issaq HJ, Schumack LJ, Grimes MK, Henderson LE, Arthur LO. 1992. Tightly bound zinc in human immunodeficiency virus type 1, human T-cell leukemia virus type I, and other retroviruses. J Virol 66:840–847. PubMed PMC

Green LM, Berg JM. 1989. A retroviral Cys-Xaa2-Cys-Xaa4-His-Xaa4-Cys peptide binds metal ions: spectroscopic studies and a proposed three-dimensional structure. Proc Natl Acad Sci U S A 86:4047–4051. PubMed PMC

Summers MF, Henderson LE, Chance MR, Bess JW Jr, South TL, Blake PR, Sagi I, Perez-Alvarado G, Sowder RC III, Hare DR. 1992. Nucleocapsid zinc fingers detected in retroviruses: EXAFS studies of intact viruses and the solution-state structure of the nucleocapsid protein from HIV-1. Protein Sci 1:563–574. doi:10.1002/pro.5560010502. PubMed DOI PMC

Ali LM, Rizvi TA, Mustafa F. 2016. Cross- and co-packaging of retroviral RNAs and their consequences. Viruses 8:E276. doi:10.3390/v8100276. PubMed DOI PMC

Morellet N, de Rocquigny H, Mely Y, Jullian N, Demene H, Ottmann M, Gerard D, Darlix JL, Fournie-Zaluski MC, Roques BP. 1994. Conformational behaviour of the active and inactive forms of the nucleocapsid NCp7 of HIV-1 studied by 1H NMR. J Mol Biol 235:287–301. doi:10.1016/S0022-2836(05)80033-6. PubMed DOI

Gao Y, Kaluarachchi K, Giedroc DP. 1998. Solution structure and backbone dynamics of Mason-Pfizer monkey virus (MPMV) nucleocapsid protein. Protein Sci 7:2265–2280. doi:10.1002/pro.5560071104. PubMed DOI PMC

D'Souza V, Summers MF. 2005. How retroviruses select their genomes. Nat Rev Microbiol 3:643–655. doi:10.1038/nrmicro1210. PubMed DOI

Johnson SF, Telesnitsky A. 2010. Retroviral RNA dimerization and packaging: the what, how, when, where, and why. PLoS Pathog 6:e1001007. doi:10.1371/journal.ppat.1001007. PubMed DOI PMC

Lever AM. 2007. HIV-1 RNA packaging. Adv Pharmacol 55:1–32. doi:10.1016/S1054-3589(07)55001-5. PubMed DOI

Jaballah SA, Aktar SJ, Ali J, Phillip PS, Al Dhaheri NS, Jabeen A, Rizvi TA. 2010. A G-C-rich palindromic structural motif and a stretch of single-stranded purines are required for optimal packaging of Mason-Pfizer monkey virus (MPMV) genomic RNA. J Mol Biol 401:996–1014. doi:10.1016/j.jmb.2010.06.043. PubMed DOI

Mustafa F, Ghazawi A, Jayanth P, Phillip PS, Ali J, Rizvi TA. 2005. Sequences intervening between the core packaging determinants are dispensable for maintaining the packaging potential and propagation of feline immunodeficiency virus transfer vector RNAs. J Virol 79:13817–13821. doi:10.1128/JVI.79.21.13817-13821.2005. PubMed DOI PMC

Keane SC, Heng X, Lu K, Kharytonchyk S, Ramakrishnan V, Carter G, Barton S, Hosic A, Florwick A, Santos J, Bolden NC, McCowin S, Case DA, Johnson BA, Salemi M, Telesnitsky A, Summers MF. 2015. Structure of the HIV-1 RNA packaging signal. Science 348:917–921. doi:10.1126/science.aaa9266. PubMed DOI PMC

Moore MD, Hu WS. 2009. HIV-1 RNA dimerization: it takes two to tango. AIDS Rev 11:91–102. PubMed PMC

Lu K, Heng X, Summers MF. 2011. Structural determinants and mechanism of HIV-1 genome packaging. J Mol Biol 410:609–633. doi:10.1016/j.jmb.2011.04.029. PubMed DOI PMC

Clever JL, Parslow TG. 1997. Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J Virol 71:3407–3414. PubMed PMC

McBride MS, Panganiban AT. 1997. Position dependence of functional hairpins important for human immunodeficiency virus type 1 RNA encapsidation in vivo. J Virol 71:2050–2058. PubMed PMC

Russell RS, Roldan A, Detorio M, Hu J, Wainberg MA, Liang C. 2003. Effects of a single amino acid substitution within the p2 region of human immunodeficiency virus type 1 on packaging of spliced viral RNA. J Virol 77:12986–12995. doi:10.1128/JVI.77.24.12986-12995.2003. PubMed DOI PMC

Luban J, Goff SP. 1994. Mutational analysis of cis-acting packaging signals in human immunodeficiency virus type 1 RNA. J Virol 68:3784–3793. PubMed PMC

McBride MS, Panganiban AT. 1996. The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J Virol 70:2963–2973. PubMed PMC

Heng X, Kharytonchyk S, Garcia EL, Lu K, Divakaruni SS, LaCotti C, Edme K, Telesnitsky A, Summers MF. 2012. Identification of a minimal region of the HIV-1 5′-leader required for RNA dimerization, NC binding, and packaging. J Mol Biol 417:224–239. doi:10.1016/j.jmb.2012.01.033. PubMed DOI PMC

Schmidt RD, Mustafa F, Lew KA, Browning MT, Rizvi TA. 2003. Sequences within both the 5′ untranslated region and the gag gene are important for efficient encapsidation of Mason-Pfizer monkey virus RNA. Virology 309:166–178. doi:10.1016/S0042-6822(02)00101-0. PubMed DOI

Aktar SJ, Vivet-Boudou V, Ali LM, Jabeen A, Kalloush RM, Richer D, Mustafa F, Marquet R, Rizvi TA. 2014. Structural basis of genomic RNA (gRNA) dimerization and packaging determinants of mouse mammary tumor virus (MMTV). Retrovirology 11:96. doi:10.1186/s12977-014-0096-6. PubMed DOI PMC

De Guzman RN, Wu ZR, Stalling CC, Pappalardo L, Borer PN, Summers MF. 1998. Structure of the HIV-1 nucleocapsid protein bound to the SL3 Ψ-RNA recognition element. Science 279:384–388. doi:10.1126/science.279.5349.384. PubMed DOI

Amarasinghe GK, De Guzman RN, Turner RB, Chancellor KJ, Wu ZR, Summers MF. 2000. NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the psi-RNA packaging signal. Implications for genome recognition. J Mol Biol 301:491–511. doi:10.1006/jmbi.2000.3979. PubMed DOI

Darlix JL, Godet J, Ivanyi-Nagy R, Fosse P, Mauffret O, Mely Y. 2011. Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J Mol Biol 410:565–581. doi:10.1016/j.jmb.2011.03.037. PubMed DOI

D'Souza V, Summers MF. 2004. Structural basis for packaging the dimeric genome of Moloney murine leukaemia virus. Nature 431:586–590. doi:10.1038/nature02944. PubMed DOI

Webb JA, Jones CP, Parent LJ, Rouzina I, Musier-Forsyth K. 2013. Distinct binding interactions of HIV-1 Gag to Psi and non-Psi RNAs: implications for viral genomic RNA packaging. RNA 19:1078–1088. doi:10.1261/rna.038869.113. PubMed DOI PMC

Wu T, Gorelick RJ, Levin JG. 2014. Selection of fully processed HIV-1 nucleocapsid protein is required for optimal nucleic acid chaperone activity in reverse transcription. Virus Res 193:52–64. doi:10.1016/j.virusres.2014.06.004. PubMed DOI PMC

Housset V, De Rocquigny H, Roques BP, Darlix JL. 1993. Basic amino acids flanking the zinc finger of Moloney murine leukemia virus nucleocapsid protein NCp10 are critical for virus infectivity. J Virol 67:2537–2545. PubMed PMC

Bohmova K, Hadravova R, Stokrova J, Tuma R, Ruml T, Pichova I, Rumlova M. 2010. Effect of dimerizing domains and basic residues on in vitro and in vivo assembly of Mason-Pfizer monkey virus and human immunodeficiency virus. J Virol 84:1977–1988. doi:10.1128/JVI.02022-09. PubMed DOI PMC

Bowzard JB, Bennett RP, Krishna NK, Ernst SM, Rein A, Wills JW. 1998. Importance of basic residues in the nucleocapsid sequence for retrovirus Gag assembly and complementation rescue. J Virol 72:9034–9044. PubMed PMC

Cimarelli A, Sandin S, Hoglund S, Luban J. 2000. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J Virol 74:3046–3057. doi:10.1128/JVI.74.7.3046-3057.2000. PubMed DOI PMC

Lee EG, Alidina A, May C, Linial ML. 2003. Importance of basic residues in binding of Rous sarcoma virus nucleocapsid to the RNA packaging signal. J Virol 77:2010–2020. doi:10.1128/JVI.77.3.2010-2020.2003. PubMed DOI PMC

Lee EG, Linial ML. 2004. Basic residues of the retroviral nucleocapsid play different roles in Gag-Gag and Gag-psi RNA interactions. J Virol 78:8486–8495. doi:10.1128/JVI.78.16.8486-8495.2004. PubMed DOI PMC

Lingappa JR, Dooher JE, Newman MA, Kiser PK, Klein KC. 2006. Basic residues in the nucleocapsid domain of Gag are required for interaction of HIV-1 Gag with ABCE1 (HP68), a cellular protein important for HIV-1 capsid assembly. J Biol Chem 281:3773–3784. doi:10.1074/jbc.M507255200. PubMed DOI

Poon DT, Wu J, Aldovini A. 1996. Charged amino acid residues of human immunodeficiency virus type 1 nucleocapsid p7 protein involved in RNA packaging and infectivity. J Virol 70:6607–6616. PubMed PMC

Berkowitz R, Fisher J, Goff SP. 1996. RNA packaging. Curr Top Microbiol Immunol 214:177–218. PubMed

Rulli SJ, Hibbert CS, Mirro J, Pederson T, Biswal S, Rein A. 2007. Selective and nonselective packaging of cellular RNAs in retrovirus particles. J Virol 81:6623–6631. doi:10.1128/JVI.02833-06. PubMed DOI PMC

Eckwahl MJ, Telesnitsky A, Wolin SL. 2016. Host RNA packaging by retroviruses: a newly synthesized story. mBio 7:e02025-. doi:10.1128/mBio.02025-15. PubMed DOI PMC

Fuzik T, Pichalova R, Schur FK, Strohalmova K, Krizova I, Hadravova R, Rumlova M, Briggs JA, Ulbrich P, Ruml T. 24 February 2016. Nucleic acid binding by Mason-Pfizer monkey virus CA promotes virus assembly and genome packaging. J Virol doi:10.1128/JVI.03197-15. PubMed DOI PMC

Rye-McCurdy T, Olson ED, Liu S, Binkley C, Reyes J-P, Thompson BR, Flanagan JM, Parent LJ, Musier-Forsyth K. 2016. Functional equivalence of retroviral MA domains in facilitating Psi RNA binding specificity by Gag. Viruses 8:E256. doi:10.3390/v8090256. PubMed DOI PMC

Sun M, Grigsby IF, Gorelick RJ, Mansky LM, Musier-Forsyth K. 2014. Retrovirus-specific differences in matrix and nucleocapsid protein-nucleic acid interactions: implications for genomic RNA packaging. J Virol 88:1271–1280. doi:10.1128/JVI.02151-13. PubMed DOI PMC

Rein A, Datta SA, Jones CP, Musier-Forsyth K. 2011. Diverse interactions of retroviral Gag proteins with RNAs. Trends Biochem Sci 36:373–380. doi:10.1016/j.tibs.2011.04.001. PubMed DOI PMC

Strohalmova-Bohmova K, Spiwok V, Lepsik M, Hadravova R, Krizova I, Ulbrich P, Pichova I, Bednarova L, Ruml T, Rumlova M. 2014. Role of Mason-Pfizer monkey virus CA-NC spacer peptide-like domain in assembly of immature particles. J Virol 88:14148–14160. doi:10.1128/JVI.02286-14. PubMed DOI PMC

Newman RM, Hall L, Connole M, Chen GL, Sato S, Yuste E, Diehl W, Hunter E, Kaur A, Miller GM, Johnson WE. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc Natl Acad Sci U S A 103:19134–19139. doi:10.1073/pnas.0605838103. PubMed DOI PMC

Brody BA, Hunter E. 1992. Mutations within the env gene of Mason-Pfizer monkey virus: effects on protein transport and SU-TM association. J Virol 66:3466–3475. PubMed PMC

Moore MD, Fu W, Nikolaitchik O, Chen J, Ptak RG, Hu W-S. 2007. Dimer initiation signal of human immunodeficiency virus type 1: its role in partner selection during RNA copackaging and its effects on recombination. J Virol 81:4002–4011. doi:10.1128/JVI.02589-06. PubMed DOI PMC

Moore MD, Nikolaitchik OA, Chen J, Hammarskjöld M-L, Rekosh D, Hu W-S. 2009. Probing the HIV-1 genomic RNA trafficking pathway and dimerization by genetic recombination and single virion analyses. PLoS Pathog 5:e1000627. doi:10.1371/journal.ppat.1000627. PubMed DOI PMC

Hendrix J, Baumgärtel V, Schrimpf W, Ivanchenko S, Digman MA, Gratton E, Kräusslich H-G, Müller B, Lamb DC. 2015. Live-cell observation of cytosolic HIV-1 assembly onset reveals RNA-interacting Gag oligomers. J Cell Biol 210:629–646. doi:10.1083/jcb.201504006. PubMed DOI PMC

Kutluay SB, Bieniasz PD. 2010. Analysis of the initiating events in HIV-1 particle assembly and genome packaging. PLoS Pathog 6:e1001200. doi:10.1371/journal.ppat.1001200. PubMed DOI PMC

Poole E, Strappe P, Mok H-P, Hicks R, Lever AML. 2005. HIV-1 Gag-RNA interaction occurs at a perinuclear/centrosomal site; analysis by confocal microscopy and FRET. Traffic 6:741–755. doi:10.1111/j.1600-0854.2005.00312.x. PubMed DOI

Ferrer M, Clerté C, Chamontin C, Basyuk E, Lainé S, Hottin J, Bertrand E, Margeat E, Mougel M. 2016. Imaging HIV-1 RNA dimerization in cells by multicolor super-resolution and fluctuation microscopies. Nucleic Acids Res 44:7922–7934. doi:10.1093/nar/gkw511. PubMed DOI PMC

Muriaux D, Mirro J, Harvin D, Rein A. 2001. RNA is a structural element in retrovirus particles. Proc Natl Acad Sci U S A 98:5246–5251. doi:10.1073/pnas.091000398. PubMed DOI PMC

Kaddis Maldonado RJ, Parent LJ. 2016. Orchestrating the selection and packaging of genomic RNA by retroviruses: an ensemble of viral and host factors. Viruses 8:E257. doi:10.3390/v8090257. PubMed DOI PMC

Choi G, Park S, Choi B, Hong ST, Lee JY, Hunter E, Rhee SS. 1999. Identification of a cytoplasmic targeting retention signal in a retroviral Gag polyprotein. J Virol 73:5431–5437. PubMed PMC

Rhee SS, Hunter E. 1990. A single amino acid substitution within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus. Cell 63:77–86. doi:10.1016/0092-8674(90)90289-Q. PubMed DOI

Sfakianos JN, LaCasse RA, Hunter E. 2003. The M-PMV cytoplasmic targeting-retention signal directs nascent Gag polypeptides to a pericentriolar region of the cell. Traffic 4:660–670. doi:10.1034/j.1600-0854.2003.00125.x. PubMed DOI

Cimarelli A, Luban J. 2000. Human immunodeficiency virus type 1 virion density is not determined by nucleocapsid basic residues. J Virol 74:6734–6740. doi:10.1128/JVI.74.15.6734-6740.2000. PubMed DOI PMC

Wu H, Mitra M, Naufer MN, McCauley MJ, Gorelick RJ, Rouzina I, Musier-Forsyth K, Williams MC. 2014. Differential contribution of basic residues to HIV-1 nucleocapsid protein's nucleic acid chaperone function and retroviral replication. Nucleic Acids Res 42:2525–2537. doi:10.1093/nar/gkt1227. PubMed DOI PMC

Krizova I, Hadravova R, Stokrova J, Gunterova J, Dolezal M, Ruml T, Rumlova M, Pichova I. 2012. The G-patch domain of Mason-Pfizer monkey virus is a part of reverse transcriptase. J Virol 86:1988–1998. doi:10.1128/JVI.06638-11. PubMed DOI PMC

Wildova M, Hadravova R, Stokrova J, Krizova I, Ruml T, Hunter E, Pichova I, Rumlova M. 2008. The effect of point mutations within the N-terminal domain of Mason-Pfizer monkey virus capsid protein on virus core assembly and infectivity. Virology 380:157–163. doi:10.1016/j.virol.2008.07.021. PubMed DOI PMC

Stansell E, Apkarian R, Haubova S, Diehl WE, Tytler EM, Hunter E. 2007. Basic residues in the Mason-Pfizer monkey virus Gag matrix domain regulate intracellular trafficking and capsid-membrane interactions. J Virol 81:8977–8988. doi:10.1128/JVI.00657-07. PubMed DOI PMC

Obr M, Hadravova R, Dolezal M, Krizova I, Papouskova V, Zidek L, Hrabal R, Ruml T, Rumlova M. 2014. Stabilization of the beta-hairpin in Mason-Pfizer monkey virus capsid protein—a critical step for infectivity. Retrovirology 11:94. doi:10.1186/s12977-014-0094-8. PubMed DOI PMC

Diehl WE, Stansell E, Kaiser SM, Emerman M, Hunter E. 2008. Identification of postentry restrictions to Mason-Pfizer monkey virus infection in New World monkey cells. J Virol 82:11140–11151. doi:10.1128/JVI.00269-08. PubMed DOI PMC

Wang GZ, Goff SP. 2015. Postentry restriction of Mason-Pfizer monkey virus in mouse cells. J Virol 89:2813–2819. doi:10.1128/JVI.03051-14. PubMed DOI PMC

Hadravova R, de Marco A, Ulbrich P, Stokrova J, Dolezal M, Pichova I, Ruml T, Briggs JA, Rumlova M. 2012. In vitro assembly of virus-like particles of a gammaretrovirus, the murine leukemia virus XMRV. J Virol 86:1297–1306. doi:10.1128/JVI.05564-11. PubMed DOI PMC

Rumlova M, Krizova I, Hadravova R, Dolezal M, Strohalmova K, Keprova A, Pichova I, Ruml T. 2014. Breast cancer-associated protein—a novel binding partner of Mason-Pfizer monkey virus protease. J Gen Virol 95:1383–1389. doi:10.1099/vir.0.064345-0. PubMed DOI

Ulbrich P, Haubova S, Nermut MV, Hunter E, Rumlova M, Ruml T. 2006. Distinct roles for nucleic acid in in vitro assembly of purified Mason-Pfizer monkey virus CANC proteins. J Virol 80:7089–7099. doi:10.1128/JVI.02694-05. PubMed DOI PMC

Humpolickova J, Mejdrova I, Matousova M, Nencka R, Boura E. 2017. Fluorescent inhibitors as tools to characterize enzymes: case study of the lipid kinase phosphatidylinositol 4-kinase IIIbeta (PI4KB). J Med Chem 60:119–127. doi:10.1021/acs.jmedchem.6b01466. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...