Host and viral determinants of Mx2 antiretroviral activity

Journal of Virology

Volumn 88, Issue 14, 2014, Pages 7738-7752

  Busnadiego, Idoia ^a   Kane, Melissa ^b   Rihn, Suzannah J ^b   Preugschas, Hannah F ^a   Hughes, Joseph ^a   Blanco Melo, Daniel ^b   Strouvelle, Victoria P ^a   Zang, Trinity M ^b,c   Willett, Brian J ^a   Boutell, Chris ^a   Bieniasz, Paul D ^b,c   Wilson, Sam J ^a  

^a MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^b ROCKEFELLER UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYXOVIRUS RESISTANCE 2 PROTEIN; TRANSCRIPTION FACTOR; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; SPECIES DIFFERENCE; VIRUS CAPSID; VIRUS INHIBITION;

ANIMALS; DNA MUTATIONAL ANALYSIS; EVOLUTION, MOLECULAR; HIV CORE PROTEIN P24; HIV-1; HUMANS; MUTAGENESIS; MYXOVIRUS RESISTANCE PROTEINS;

EID: 84904684665     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00214-14     Document Type: Article

References (82)

1. Ho DD, Hartshorn KL, Rota TR, Andrews CA, Kaplan JC, Schooley RT, Hirsch MS. 1985. Recombinant human interferon alfa-A suppresses HTLV-III replication in vitro. Lancet i:602-604.
2. Asmuth DM, Murphy RL, Rosenkranz SL, Lertora JJ, Kottilil S, Cramer Y, Chan ES, Schooley RT, Rinaldo CR, Thielman N, Li XD, Wahl SM, Shore J, Janik J, Lempicki RA, Simpson Y, Pollard RB. 2010. Safety, tolerability, and mechanisms of antiretroviral activity of pegylated interferon alfa-2a in HIV-1-monoinfected participants: a phase II clinical trial. J. Infect. Dis. 201:1686-1696. http://dx.doi.org/10.1086/652420.
3. Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS, O'Connor S, Marx PA, Meythaler M, Goldstein S, Buckler-White A, Kaur A, Hirsch VM, Johnson WE. 2010. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol. 8:1-12. http://dx.doi.org/10.1371 /journal.pbio.1000462.
4. Liberatore RA, Bieniasz PD. 2011. Tetherin is a key effector of the antiretroviral activity of type I interferon in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 108:18097-18101. http://dx.doi.org/10.1073 /pnas.1113694108.
5. Okeoma CM, Lovsin N, Peterlin BM, Ross SR. 2007. APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 445:927-930. http://dx.doi.org/10.1038/nature05540.
6. Hrecka K, Hao C, Gierszewska M, Swanson SK, Kesik-Brodacka M, Srivastava S, Florens L, Washburn MP, Skowronski J. 2011. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 474:658-661. http://dx.doi.org/10.1038/nature10195.
7. Laguette N, Sobhian B, Casartelli N, Ringeard M, Chable-Bessia C, Segeral E, Yatim A, Emiliani S, Schwartz O, Benkirane M. 2011. SAMHD1 is the dendritic-and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474:654-657. http://dx.doi.org/10.1038/nature10117.
8. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430. http://dx.doi.org /10.1038/nature06553.
9. Sheehy AM, Gaddis NC, Choi JD, Malim MH. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650. http://dx.doi.org/10.1038/nature00939.
10. Wilson SJ, Schoggins JW, Zang T, Kutluay SB, Jouvenet N, Alim MA, Bitzegeio J, Rice CM, Bieniasz PD. 2012. Inhibition of HIV-1 particle assembly by 2',3'-cyclic-nucleotide 3'-phosphodiesterase. Cell Host Microbe 12:585-597. http://dx.doi.org/10.1016/j.chom.2012.08.012.
11. Gao G, Guo X, Goff SP. 2002. Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297:1703-1706. http://dx.doi.org/10.1126/science.1074276.
12. Furtak V, Mulky A, Rawlings SA, Kozhaya L, Lee K, Kewalramani VN, Unutmaz D. 2010. Perturbation of the P-body component Mov10 inhibits HIV-1 infectivity. PLoS One 5:e9081. http://dx.doi.org/10.1371/journal.pone.0009081.
13. Goujon C, Schaller T, Galao RP, Amie SM, Kim B, Olivieri K, Neil SJ, Malim MH. 2013. Evidence for IFNα-induced, SAMHD1-independent inhibitors of early HIV-1 infection. Retrovirology 10:23. http://dx.doi.org /10.1186/1742-4690-10-23.
14. Lindenmann J. 1962. Resistance of mice to mouse-adapted influenza A virus. Virology 16:203-204. http://dx.doi.org/10.1016/0042-6822(62)90297-0.
15. Staeheli P, Haller O, Boll Lindenmann WJ, Weissmann C. 1986. Mx protein: constitutive expression in 3T3 cells transformed with cloned Mx cDNA confers selective resistance to influenza virus. Cell 44:147-158. http://dx.doi.org/10.1016/0092-8674(86)90493-9.
16. King MC, Raposo G, Lemmon MA. 2004. Inhibition of nuclear import and cell-cycle progression by mutated forms of the dynamin-like GTPase MxB. Proc. Natl. Acad. Sci. U. S. A. 101:8957-8962. http://dx.doi.org/10.1073/pnas.0403167101.
17. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485. http://dx.doi.org/10.1038/nature09907.
18. Kane M, Yadav SS, Bitzegeio J, Kutluay SB, Zang T, Wilson SJ, Schoggins JW, Rice CM, Yamashita M, Hatziioannou T, Bieniasz PD. 2013. MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 502: 563-566. http://dx.doi.org/10.1038/nature12653.
19. Goujon C, Moncorge O, Bauby H, Doyle T, Ward CC, Schaller T, Hue S, Barclay WS, Schulz R, Malim MH. 2013. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502:559-562. http://dx.doi.org/10.1038/nature12542.
20. Liu Z, Pan Q, Ding S, Qian J, Xu F, Zhou J, Cen S, Guo F, Liang C. 2013. The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 14:398-410. http://dx.doi.org/10.1016/j.chom.2013.08.015.
21. Wiederschain D, Wee S, Chen L, Loo A, Yang G, Huang A, Chen Y, Caponigro G, Yao YM, Lengauer C, Sellers WR, Benson JD. 2009. Single-vector inducible lentiviral RNAi system for oncology target validation. Cell Cycle 8:498-504. http://dx.doi.org/10.4161/cc.8.3.7701.
22. Everett RD, Parsy ML, Orr A. 2009. Analysis of the functions of herpes simplex virus type 1 regulatory protein ICP0 that are critical for lytic infection and derepression of quiescent viral genomes. J. Virol. 83:4963-4977. http://dx.doi.org/10.1128/JVI.02593-08.
23. Arnaud F, Black SG, Murphy L, Griffiths DJ, Neil SJ, Spencer TE, Palmarini M. 2010. Interplay between ovine bone marrow stromal cell antigen 2/tetherin and endogenous retroviruses. J. Virol. 84:4415-4425. http://dx.doi.org/10.1128/JVI.00029-10.
24. Tebit DM, Zekeng L, Kaptue L, Gurtler L, Fackler OT, Keppler OT, Herchenroder O, Krausslich HG. 2004. Construction and characterization of an HIV-1 group O infectious molecular clone and analysis of vprand nef-negative derivatives. Virology 326:329-339. http://dx.doi.org/10.1016/j.virol.2004.05.027.
25. Wilson SJ, Webb BL, Ylinen LM, Verschoor E, Heeney JL, Towers GJ. 2008. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. U. S. A. 105:3557-3562. http://dx.doi.org/10.1073/pnas.0709003105.
26. Virgen CA, Kratovac Z, Bieniasz PD, Hatziioannou T. 2008. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc. Natl. Acad. Sci. U. S. A. 105:3563-3568. http://dx.doi.org/10.1073/pnas.0709258105.
27. Rihn SJ, Wilson SJ, Loman NJ, Alim M, Bakker SE, Bhella D, Gifford RJ, Rixon FJ, Bieniasz PD. 2013. Extreme genetic fragility of the HIV-1 capsid. PLoS Pathog. 9:e1003461. http://dx.doi.org/10.1371/journal.ppat.1003461.
28. Soll SJ, Wilson SJ, Kutluay SB, Hatziioannou T, Bieniasz PD. 2013. Assisted evolution enables HIV-1 to overcome a high TRIM5α-imposed genetic barrier to rhesus macaque tropism. PLoS Pathog. 9:e1003667. http://dx.doi.org/10.1371/journal.ppat.1003667.
29. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning, vol 2. Cold Spring Harbor Laboratory Press, New York, NY.
30. Jouvenet N, Neil SJ, Bess C, Johnson MC, Virgen CA, Simon SM, Bieniasz PD. 2006. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4:e435. http://dx.doi.org/10.1371/journal.pbio.0040435.
31. 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. http: //dx.doi.org/10.1016/j.cell.2009.04.063.
32. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7:539. http://dx.doi.org/10.1038/msb.2011.75.
33. Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34:W609-W612. http://dx.doi.org/10.1093 /nar/gkl315.
34. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772. http: //dx.doi.org/10.1038/nmeth.2111.
35. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704. http://dx.doi.org/10.1080/10635150390235520.
36. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. 2010. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455-2457. http://dx.doi.org/10.1093/bioinformatics /btq429.
37. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. (Camb.) 13:555-556.
38. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
39. Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD. 2004. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5α. Proc. Natl. Acad. Sci. U. S. A. 101:10774-10779. http: //dx.doi.org/10.1073/pnas.0402361101.
40. Ohkura S, Goldstone DC, Yap MW, Holden-Dye K, Taylor IA, Stoye JP. 2011. Novel escape mutants suggest an extensive TRIM5α binding site spanning the entire outer surface of the murine leukemia virus capsid protein. PLoS Pathog. 7:e1002011. http://dx.doi.org/10.1371 /journal.ppat.1002011.
41. Sebastian S, Luban J. 2005. TRIM5α selectively binds a restrictionsensitive retroviral capsid. Retrovirology 2:40. http://dx.doi.org/10.1186 /1742-4690-2-40.
42. Sawyer SL, Wu LI, Emerman M, Malik HS. 2005. Positive selection of primate TRIM5α identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. U. S. A. 102:2832-2837. http://dx.doi.org /10.1073/pnas.0409853102.
43. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, Johnson MC, Munch J, Kirchhoff F, Bieniasz PD, Hatziioannou T. 2009. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6:54-67. http://dx.doi.org/10.1016/j.chom.2009.05.008.
44. Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT. 2009. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS pathogens 5:e1000429. http://dx.doi.org/10.1371/journal.ppat.1000429.
45. Zhang F, Landford WN, Ng M, McNatt MW, Bieniasz PD, Hatziioannou T. 2011. SIV Nef proteins recruit the AP-2 complex to antagonize Tetherin and facilitate virion release. PLoS Pathog. 7:e1002039. http://dx.doi.org/10.1371/journal.ppat.1002039.
46. Serra-Moreno R, Zimmermann K, Stern LJ, Evans DT. 2013. Tetherin/BST-2 antagonism by Nef depends on a direct physical interaction between Nef and tetherin, and on clathrin-mediated endocytosis. PLoS Pathog. 9:e1003487. http://dx.doi.org/10.1371/journal.ppat.1003487.
47. Ko JH, Jin HK, Asano A, Takada A, Ninomiya A, Kida H, Hokiyama H, Ohara M, Tsuzuki M, Nishibori M, Mizutani M, Watanabe T. 2002. Polymorphisms and the differential antiviral activity of the chicken Mx gene. Genome Res. 12:595-601. http://dx.doi.org/10.1101/gr.210702.
48. Larsen R, Rokenes TP, Robertsen B. 2004. Inhibition of infectious pancreatic necrosis virus replication by Atlantic salmon Mx1 protein. J. Virol. 78:7938-7944. http://dx.doi.org/10.1128/JVI.78.15.7938-7944.2004.
49. 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 TRIM5α. Proc. Natl. Acad. Sci. U. S. A. 103:19134-19139. http://dx.doi.org/10.1073/pnas.0605838103.
50. Song C, Hunter E. 2003. Variable sensitivity to substitutions in the Nterminal heptad repeat of Mason-Pfizer monkey virus transmembrane protein. J. Virol. 77:7779-7785. http://dx.doi.org/10.1128/JVI.77.14.7779-7785.2003.
51. Lee YN, Bieniasz PD. 2007. Reconstitution of an infectious human en-dogenous retrovirus. PLoS Pathog. 3:e10. http://dx.doi.org/10.1371 /journal.ppat.0030010.
52. Melen K, Keskinen P, Ronni T, Sareneva T, Lounatmaa K, Julkunen I. 1996. Human MxB protein, an interferon-alpha-inducible GTPase, contains a nuclear targeting signal and is localized in the heterochromatin region beneath the nuclear envelope. J. Biol. Chem. 271:23478-23486. http://dx.doi.org/10.1074/jbc.271.38.23478.
53. Ptak RG, Gallay PA, Jochmans D, Halestrap AP, Ruegg UT, Pallansch LA, Bobardt MD, de Bethune MP, Neyts J, De Clercq E, Dumont JM, Scalfaro P, Besseghir K, Wenger RM, Rosenwirth B. 2008. Inhibition of human immunodeficiency virus type 1 replication in human cells by Debio-025, a novel cyclophilin binding agent. Antimicrob. Agents Chemother. 52:1302-1317. http://dx.doi.org/10.1128/AAC.01324-07.
54. Newman RM, Hall L, Kirmaier A, Pozzi LA, Pery E, Farzan M, O'Neil SP, Johnson W. 2008. Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog. 4:e1000003. http://dx.doi.org/10.1371 /journal.ppat.1000003.
55. Yamashita M, Perez O, Hope TJ, Emerman M. 2007. Evidence for direct involvement of the capsid protein in HIV infection of nondividing cells. PLoS Pathog. 3:1502-1510. http://dx.doi.org/10.1371/journal.ppat.0030156.
56. McCarthy KR, Schmidt AG, Kirmaier A, Wyand AL, Newman RM, Johnson WE. 2013. Gain-of-sensitivity mutations in a Trim5-resistant primary isolate of pathogenic SIV identify two independent conserved determinants of Trim5α specificity. PLoS Pathog. 9:e1003352. http://dx.doi.org/10.1371/journal.ppat.1003352.
57. 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. http://dx.doi.org/10.1038/nature12162.
58. Forshey BM, von Schwedler U, Sundquist WI, Aiken C. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76:5667-5677. http://dx.doi.org/10.1128/JVI.76.11.5667-5677.2002.
59. Lee K, Ambrose Z, Martin TD, Oztop I, Mulky A, Julias JG, Vandegraaff N, Baumann JG, Wang R, Yuen W, Takemura T, Shelton K, Taniuchi I, Li Y, Sodroski J, Littman DR, Coffin JM, Hughes SH, Unutmaz D, Engelman A, KewalRamani VN. 2010. Flexible use of nuclear import pathways by HIV-1. Cell Host Microbe 7:221-233. http: //dx.doi.org/10.1016/j.chom.2010.02.007.
60. Krishnan L, Matreyek KA, Oztop I, Lee K, Tipper CH, Li X, Dar MJ, Kewalramani VN, Engelman A. 2010. The requirement for cellular transportin 3 (TNPO3 or TRN-SR2) during infection maps to human immunodeficiency virus type 1 capsid and not integrase. J. Virol. 84:397-406. http://dx.doi.org/10.1128/JVI.01899-09.
61. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, Hue S, Fletcher AJ, Lee K, KewalRamani VN, Noursadeghi M, Jenner RG, James LC, Bushman FD, Towers GJ. 2011. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting, and replication efficiency. PLoS Pathog. 7:e1002439. http://dx.doi.org/10.1371/journal.ppat.1002439.
62. Mitchell PS, Patzina C, Emerman M, Haller O, Malik HS, Kochs G. 2012. Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12:598-604. http://dx.doi.org/10.1016/j.chom.2012.09.005.
63. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Fofana IB, Johnson WE, Neil SJ, Bieniasz PD. 2009. Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog. 5:e1000300. http://dx.doi.org/10.1371/journal.ppat.1000300.
64. Turan K, Mibayashi M, Sugiyama K, Saito S, Numajiri A, Nagata K. 2004. Nuclear MxA proteins form a complex with influenza virus NP and inhibit the transcription of the engineered influenza virus genome. Nucleic Acids Res. 32:643-652. http://dx.doi.org/10.1093/nar/gkh192.
65. Kochs G, Haller O. 1999. GTP-bound human MxA protein interacts with the nucleocapsids of Thogoto virus (Orthomyxoviridae). J. Biol. Chem. 274:4370-4376. http://dx.doi.org/10.1074/jbc.274.7.4370.
66. Gao S, von der Malsburg A, Paeschke S, Behlke J, Haller O, Kochs G, Daumke O. 2010. Structural basis of oligomerization in the stalk region of dynamin-like MxA. Nature 465:502-506. http://dx.doi.org/10.1038 /nature08972.
67. Haller O. 2013. Dynamins are forever: MxB inhibits HIV-1. Cell Host Microbe 14:371-373. http://dx.doi.org/10.1016/j.chom.2013.10.002.
68. Ganser-Pornillos BK, Chandrasekaran V, Pornillos O, Sodroski JG, Sundquist WI, Yeager M. 2011. Hexagonal assembly of a restricting TRIM5α protein. Proc. Natl. Acad. Sci. U. S. A. 108:534-539. http://dx.doi.org/10.1073/pnas.1013426108.
69. Yang H, Ji X, Zhao G, Ning J, Zhao Q, Aiken C, Gronenborn AM, Zhang P, Xiong Y. 2012. Structural insight into HIV-1 capsid recognition by rhesus TRIM5α. Proc. Natl. Acad. Sci. U. S. A. 109:18372-18377. http: //dx.doi.org/10.1073/pnas.1210903109.
70. Price AJ, Fletcher AJ, Schaller T, Elliott T, Lee K, KewalRamani VN, Chin JW, Towers GJ, James LC. 2012. CPSF6 defines a conserved capsid interface that modulates HIV-1 replication. PLoS Pathog. 8:e1002896. http://dx.doi.org/10.1371/journal.ppat.1002896.
71. Matreyek KA, Yucel SS, Li X, Engelman A. 2013. Nucleoporin NUP153 phenylalanine-glycine motifs engage a common binding pocket within the HIV-1 capsid protein to mediate lentiviral infectivity. PLoS Pathog. 9:e1003693. http://dx.doi.org/10.1371/journal.ppat.1003693.
72. Ylinen LM, Schaller T, Price A, Fletcher AJ, Noursadeghi M, James LC, Towers GJ. 2009. Cyclophilin A levels dictate infection efficiency of human immunodeficiency virus type 1 capsid escape mutants A92E and G94D. J. Virol. 83:2044-2047. http://dx.doi.org/10.1128/JVI.01876-08.
73. Fenton-May AE, Dibben O, Emmerich T, Ding H, Pfafferott K, Aasa-Chapman MM, Pellegrino P, Williams I, Cohen MS, Gao F, Shaw GM, Hahn BH, Ochsenbauer C, Kappes JC, Borrow P. 2013. Relative resistance of HIV-1 founder viruses to control by interferon-alpha. Retrovirology 10:146. http://dx.doi.org/10.1186/1742-4690-10-146.
74. Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, Zajic L, Iyer SS, Decker JM, Kumar A, Hora B, Berg A, Cai F, Hopper J, Denny TN, Ding H, Ochsenbauer C, Kappes JC, Galimidi RP, West AP, Jr, Bjorkman PJ, Wilen CB, Doms RW, O'Brien M, Bhardwaj N, Borrow P, Haynes BF, Muldoon M, Theiler JP, Korber B, Shaw GM, Hahn BH. 2013. Phenotypic properties of transmitted founder HIV-1. Proc. Natl. Acad. Sci. U. S. A. 110: 6626-6633. http://dx.doi.org/10.1073/pnas.1304288110.
75. Manel N, Hogstad B, Wang Y, Levy DE, Unutmaz D, Littman DR. 2010. Acryptic sensor for HIV-1 activates antiviral innate immunity in dendritic cells. Nature 467:214-217. http://dx.doi.org/10.1038/nature09337.
76. Rasaiyaah J, Tan CP, Fletcher AJ, Price AJ, Blondeau C, Hilditch L, Jacques DA, Selwood DL, James LC, Noursadeghi M, Towers GJ. 2013. HIV-1 evades innate immune recognition through specific cofactor recruitment. Nature 503:402-405. http://dx.doi.org/10.1038/nature12769.
77. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. 1994. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68:6103-6110.
78. Dahirel V, Shekhar K, Pereyra F, Miura T, Artyomov M, Talsania S, Allen TM, Altfeld M, Carrington M, Irvine DJ, Walker BD, Chakraborty AK. 2011. Coordinate linkage of HIV evolution reveals regions of immunological vulnerability. Proc. Natl. Acad. Sci. U. S. A. 108: 11530-11535. http://dx.doi.org/10.1073/pnas.1105315108.
79. Brockman MA, Brumme ZL, Brumme CJ, Miura T, Sela J, Rosato PC, Kadie CM, Carlson JM, Markle TJ, Streeck H, Kelleher AD, Markowitz M, Jessen H, Rosenberg E, Altfeld M, Harrigan PR, Heckerman D, Walker BD, Allen TM. 2010. Early selection in Gag by protective HLA alleles contributes to reduced HIV-1 replication capacity that may be largely compensated for in chronic infection. J. Virol. 84:11937-11949. http://dx.doi.org/10.1128/JVI.01086-10.
80. International HIVCS, Pereyra F, Jia X, McLaren PJ, Telenti A, de Bakker PI, Walker BD, Ripke S, Brumme CJ, Pulit SL, Carrington M, Kadie CM, Carlson JM, Heckerman D, Graham RR, Plenge RM, Deeks SG, Gianniny L, Crawford G, Sullivan J, Gonzalez E, Davies L, Camargo A, Moore JM, Beattie N, Gupta S, Crenshaw A, Burtt NP, Guiducci C, Gupta N, Gao X, Qi Y, Yuki Y, Piechocka-Trocha A, Cutrell E, Rosenberg R, Moss KL, Lemay P, O'Leary J, Schaefer T, Verma P, Toth I, Block B, Baker B, Rothchild A, Lian J, Proudfoot J, Alvino DM, et al. 2010. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330:1551-1557. http://dx.doi.org/10.1126 /science.1195271.
81. Demaison C, Parsley K, Brouns G, Scherr M, Battmer K, Kinnon C, Grez M, Thrasher AJ. 2002. High-level transduction and gene expression in hematopoietic repopulating cells using a human immunodeficiency virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum. Gene Ther. 13:803-813. http://dx.doi.org /10.1089/10430340252898984.
82. Saenz DT, Poeschla EM. 2004. FIV: from lentivirus to lentivector. J. Gene Med. 6(Suppl 1):S95-S104.