Antithetic effect of interferon-α on cell-free and cell-to-cell HIV-1 infection

1.

Gray RH, Wawer MJ, Brookmeyer R, Sewankambo NK, Serwadda D, Wabwire-Mangen F, et al. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in

Rakai, Uganda. Lancet. 2001; 357(9263):1149–53. Epub 2001/04/27. https://doi.org/10.1016/S01406736(00)04331-2 PMID: 11323041.

2.

Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1

infection. J Exp Med. 2009; 206(6):1273–89. Epub 2009/06/03. https://doi.org/10.1084/jem.20090378

PMID: 19487424; PubMed Central PMCID: PMC2715054.

3.

Pilcher CD, Fiscus SA, Nguyen TQ, Foust E, Wolf L, Williams D, et al. Detection of acute infections

during HIV testing in North Carolina. N Engl J Med. 2005; 352(18):1873–83. Epub 2005/05/06. https://

doi.org/10.1056/NEJMoa042291 PMID: 15872202.

4.

Talbert-Slagle K, Atkins KE, Yan KK, Khurana E, Gerstein M, Bradley EH, et al. Cellular superspreaders: an epidemiological perspective on HIV infection inside the body. PLoS Pathog. 2014; 10(5):

e1004092. Epub 2014/05/09. https://doi.org/10.1371/journal.ppat.1004092 PMID: 24811311; PubMed

Central PMCID: PMC4014458.

5.

Iyer SS, Bibollet-Ruche F, Sherrill-Mix S, Learn GH, Plenderleith L, Smith AG, et al. Resistance to type

1 interferons is a major determinant of HIV-1 transmission fitness. Proc Natl Acad Sci U S A. 2017;

114(4):E590–E9. Epub 2017/01/11. https://doi.org/10.1073/pnas.1620144114 PMID: 28069935;

PubMed Central PMCID: PMC5278458.

6.

Parrish NF, Gao F, Li H, Giorgi EE, Barbian HJ, Parrish EH, et al. Phenotypic properties of transmitted

founder HIV-1. Proc Natl Acad Sci U S A. 2013; 110(17):6626–33. Epub 2013/04/02. https://doi.org/

10.1073/pnas.1304288110 PMID: 23542380; PubMed Central PMCID: PMC3637789.

7.

Carlson JM, Schaefer M, Monaco DC, Batorsky R, Claiborne DT, Prince J, et al. HIV transmission.

Selection bias at the heterosexual HIV-1 transmission bottleneck. Science. 2014; 345(6193):1254031.

Epub 2014/07/12. https://doi.org/10.1126/science.1254031 PMID: 25013080; PubMed Central

PMCID: PMC4289910.

8.

Fenton-May AE, Dibben O, Emmerich T, Ding H, Pfafferott K, Aasa-Chapman MM, et al. Relative

resistance of HIV-1 founder viruses to control by interferon-α. Retrovirology. 2013; 10:146. Epub

2013/12/05. https://doi.org/10.1186/1742-4690-10-146 PMID: 24299076; PubMed Central PMCID:

PMC3907080.

9.

Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010; 140(6):805–20.

Epub 2010/03/23. https://doi.org/10.1016/j.cell.2010.01.022 PMID: 20303872.

10.

Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006; 124(4):783–

801. Epub 2006/02/25. https://doi.org/10.1016/j.cell.2006.02.015 PMID: 16497588.

11.

Kawai T, Akira S. Innate immune recognition of viral infection. Nat Immunol. 2006; 7(2):131–7. Epub

2006/01/21. https://doi.org/10.1038/ni1303 PMID: 16424890.

12.

Soper A, Kimura I, Nagaoka S, Konno Y, Yamamoto K, Koyanagi Y, et al. Type I interferon responses

by HIV-1 infection: association with disease progression and control. Front Immunol. 2017; 8:1823.

https://doi.org/10.3389/fimmu.2017.01823 PMID: 29379496; PubMed Central PMCID: PMC5775519.

13.

Kluge SF, Sauter D, Kirchhoff F. SnapShot: antiviral restriction factors. Cell. 2015; 163(3):774–e1.

Epub 2015/10/27. https://doi.org/10.1016/j.cell.2015.10.019 PMID: 26496613.

14.

Doyle T, Goujon C, Malim MH. HIV-1 and interferons: who’s interfering with whom? Nat Rev Microbiol.

2015; 13(7):403–13. Epub 2015/04/29. https://doi.org/10.1038/nrmicro3449 PMID: 25915633.

15.

Agosto LM, Uchil PD, Mothes W. HIV cell-to-cell transmission: effects on pathogenesis and antiretroviral therapy. Trends Microbiol. 2015; 23(5):289–95. Epub 2015/03/15. https://doi.org/10.1016/j.tim.

2015.02.003 PMID: 25766144; PubMed Central PMCID: PMC4417442.

16.

Martin N, Sattentau Q. Cell-to-cell HIV-1 spread and its implications for immune evasion. Curr Opin

HIV AIDS. 2009; 4(2):143–9. Epub 2009/04/03. https://doi.org/10.1097/COH.0b013e328322f94a

PMID: 19339954.

17.

Sattentau Q. Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol. 2008; 6

(11):815–26. Epub 2008/10/17. https://doi.org/10.1038/nrmicro1972 PMID: 18923409.

18.

Graw F, Perelson AS. Modeling Viral Spread. Annu Rev Virol. 2016; 3(1):555–72. Epub 2016/09/13.

https://doi.org/10.1146/annurev-virology-110615-042249 PMID: 27618637; PubMed Central PMCID:

PMC5072357.

19.

Iwami S, Takeuchi JS, Nakaoka S, Mammano F, Clavel F, Inaba H, et al. Cell-to-cell infection by HIV

contributes over half of virus infection. Elife. 2015; 4. https://doi.org/10.7554/eLife.08150 PMID:

26441404; PubMed Central PMCID: PMC4592948.

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010053 April 25, 2022

22 / 27

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Antithetic effect of interferon-α on cell-free and cell-to-cell HIV-1 infection

20.

Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, et al. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol. 1986; 59(2):284–91. Epub 1986/08/01. PubMed Central PMCID:

PMC253077. https://doi.org/10.1128/JVI.59.2.284-291.1986 PMID: 3016298

21.

Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O. Inefficient human immunodeficiency

virus replication in mobile lymphocytes. J Virol. 2007; 81(2):1000–12. Epub 2006/11/03. https://doi.

org/10.1128/JVI.01629-06 PMID: 17079292; PubMed Central PMCID: PMC1797449.

22.

Goujon C, Malim MH. Characterization of the alpha interferon-induced postentry block to HIV-1 infection in primary human macrophages and T cells. J Virol. 2010; 84(18):9254–66. Epub 2010/07/09.

https://doi.org/10.1128/JVI.00854-10 PMID: 20610724; PubMed Central PMCID: PMC2937661.

23.

Neil SJ, Sandrin V, Sundquist WI, Bieniasz PD. An interferon-alpha-induced tethering mechanism

inhibits HIV-1 and Ebola virus particle release but is counteracted by the HIV-1 Vpu protein. Cell Host

Microbe. 2007; 2(3):193–203. https://doi.org/10.1016/j.chom.2007.08.001 PMID: 18005734; PubMed

Central PMCID: PMC3793644.

24.

Lodermeyer V, Suhr K, Schrott N, Kolbe C, Sturzel CM, Krnavek D, et al. 90K, an interferon-stimulated

gene product, reduces the infectivity of HIV-1. Retrovirology. 2013; 10:111. Epub 20131024. https://

doi.org/10.1186/1742-4690-10-111 PMID: 24156545; PubMed Central PMCID: PMC3827937.

25.

Dillon SM, Guo K, Austin GL, Gianella S, Engen PA, Mutlu EA, et al. A compartmentalized type I interferon response in the gut during chronic HIV-1 infection is associated with immunopathogenesis.

AIDS. 2018; 32(12):1599–611. https://doi.org/10.1097/QAD.0000000000001863 PMID: 29762170;

PubMed Central PMCID: PMC6054446.

26.

Hardy GA, Sieg S, Rodriguez B, Anthony D, Asaad R, Jiang W, et al. Interferon-alpha is the primary

plasma type-I IFN in HIV-1 infection and correlates with immune activation and disease markers.

PLoS One. 2013; 8(2):e56527. Epub 20130220. https://doi.org/10.1371/journal.pone.0056527 PMID:

23437155; PubMed Central PMCID: PMC3577907.

27.

Ikeda H, Godinho-Santos A, Rato S, Vanwalscappel B, Clavel F, Aihara K, et al. Quantifying the antiviral effect of IFN on HIV-1 replication in cell culture. Sci Rep. 2015; 5:11761. Epub 2015/06/30. https://

doi.org/10.1038/srep11761 PMID: 26119462; PubMed Central PMCID: PMC4483772.

28.

Neumann A, Polis M, Rozenberg L, Jackson J, Reitano K, McLaughlin M, et al. Differential antiviral

effect of PEG-interferon-α-2b on HIV and HCV in the treatment of HIV/HCV co-infected patients.

AIDS. 2007; 21(14):1855–65. Epub 2007/08/28. https://doi.org/10.1097/QAD.0b013e32825eaba7

PMID: 17721093.

29.

Harper MS, Guo K, Gibbert K, Lee EJ, Dillon SM, Barrett BS, et al. Interferon-α subtypes in an ex vivo

model of acute HIV-1 infection: expression, potency and effector mechanisms. PLoS Pathog. 2015; 11

(11):e1005254. Epub 2015/11/04. https://doi.org/10.1371/journal.ppat.1005254 PMID: 26529416;

PubMed Central PMCID: PMC4631339.

30.

Schoggins JW. Interferon-stimulated genes: roles in viral pathogenesis. Curr Opin Virol. 2014; 6:40–6.

Epub 2014/04/10. https://doi.org/10.1016/j.coviro.2014.03.006 PMID: 24713352; PubMed Central

PMCID: PMC4077717.

31.

Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host

defenses. Annu Rev Immunol. 2014; 32:513–45. Epub 2014/02/22. https://doi.org/10.1146/annurevimmunol-032713-120231 PMID: 24555472; PubMed Central PMCID: PMC4313732.

32.

Kane M, Yadav SS, Bitzegeio J, Kutluay SB, Zang T, Wilson SJ, et al. MX2 is an interferon-induced

inhibitor of HIV-1 infection. Nature. 2013; 502(7472):563–6. Epub 2013/10/15. https://doi.org/10.1038/

nature12653 PMID: 24121441; PubMed Central PMCID: PMC3912734.

33.

Goujon C, Moncorge O, Bauby H, Doyle T, Ward CC, Schaller T, et al. Human MX2 is an interferoninduced post-entry inhibitor of HIV-1 infection. Nature. 2013; 502(7472):559–62. Epub 2013/09/21.

https://doi.org/10.1038/nature12542 PMID: 24048477; PubMed Central PMCID: PMC3808269.

34.

Foster TL, Wilson H, Iyer SS, Coss K, Doores K, Smith S, et al. Resistance of transmitted founder

HIV-1 to IFITM-mediated restriction. Cell Host Microbe. 2016; 20(4):429–42. Epub 2016/09/20. https://

doi.org/10.1016/j.chom.2016.08.006 PMID: 27640936; PubMed Central PMCID: PMC5075283.

35.

Compton AA, Bruel T, Porrot F, Mallet A, Sachse M, Euvrard M, et al. IFITM proteins incorporated into

HIV-1 virions impair viral fusion and spread. Cell Host Microbe. 2014; 16(6):736–47. Epub 2014/12/04.

https://doi.org/10.1016/j.chom.2014.11.001 PMID: 25464829.

36.

Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, et al. The interferoninduced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral

Vpu protein. Cell Host Microbe. 2008; 3(4):245–52. Epub 2008/03/18. https://doi.org/10.1016/j.chom.

2008.03.001 PMID: 18342597; PubMed Central PMCID: PMC2474773.

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010053 April 25, 2022

23 / 27

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Antithetic effect of interferon-α on cell-free and cell-to-cell HIV-1 infection

37.

Neil SJ, Zang T, Bieniasz PD. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu.

Nature. 2008; 451(7177):425–30. Epub 2008/01/18. https://doi.org/10.1038/nature06553 PMID:

18200009.

38.

Kane M, Zang TM, Rihn SJ, Zhang F, Kueck T, Alim M, et al. Identification of Interferon-Stimulated

Genes with Antiretroviral Activity. Cell Host Microbe. 2016; 20(3):392–405. Epub 2016/09/16. https://

doi.org/10.1016/j.chom.2016.08.005 PMID: 27631702; PubMed Central PMCID: PMC5026698.

39.

Yamasoba D, Sato K, Ichinose T, Imamura T, Koepke L, Joas S, et al. N4BP1 restricts HIV-1 and its

inactivation by MALT1 promotes viral reactivation. Nat Microbiol. 2019. Epub 2019/05/28. https://doi.

org/10.1038/s41564-019-0460-3 PMID: 31133753.

40.

Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, et al. Identification

and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc

Natl Acad Sci U S A. 2008; 105(21):7552–7. Epub 2008/05/21. https://doi.org/10.1073/pnas.

0802203105 PMID: 18490657; PubMed Central PMCID: PMC2387184.

41.

Mar KB, Rinkenberger NR, Boys IN, Eitson JL, McDougal MB, Richardson RB, et al. LY6E mediates

an evolutionarily conserved enhancement of virus infection by targeting a late entry step. Nat Commun. 2018; 9(1):3603. Epub 2018/09/08. https://doi.org/10.1038/s41467-018-06000-y PMID:

30190477; PubMed Central PMCID: PMC6127192.

42.

Yu J, Liang C, Liu SL. Interferon-inducible LY6E Protein Promotes HIV-1 Infection. J Biol Chem. 2017;

292(11):4674–85. Epub 2017/01/29. https://doi.org/10.1074/jbc.M116.755819 PMID: 28130445;

PubMed Central PMCID: PMC5377782.

43.

Hackett BA, Cherry S. Flavivirus internalization is regulated by a size-dependent endocytic pathway.

Proc Natl Acad Sci U S A. 2018; 115(16):4246–51. Epub 2018/04/04. https://doi.org/10.1073/pnas.

1720032115 PMID: 29610346; PubMed Central PMCID: PMC5910848.

44.

Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, et al. A diverse range of gene

products are effectors of the type I interferon antiviral response. Nature. 2011; 472(7344):481–5. Epub

2011/04/12. https://doi.org/10.1038/nature09907 PMID: 21478870; PubMed Central PMCID:

PMC3409588.

45.

Krishnan MN, Ng A, Sukumaran B, Gilfoy FD, Uchil PD, Sultana H, et al. RNA interference screen for

human genes associated with West Nile virus infection. Nature. 2008; 455(7210):242–5. Epub 2008/

08/12. https://doi.org/10.1038/nature07207 PMID: 18690214; PubMed Central PMCID:

PMC3136529.

46.

Browne EP, Letham B, Rudin C. A Computational Model of Inhibition of HIV-1 by Interferon-Alpha.

PLoS One. 2016; 11(3):e0152316. Epub 2016/03/25. https://doi.org/10.1371/journal.pone.0152316

PMID: 27010978; PubMed Central PMCID: PMC4807028.

47.

Ribeiro RM, Qin L, Chavez LL, Li D, Self SG, Perelson AS. Estimation of the initial viral growth rate

and basic reproductive number during acute HIV-1 infection. J Virol. 2010; 84(12):6096–102. Epub

2010/04/02. https://doi.org/10.1128/JVI.00127-10 PMID: 20357090; PubMed Central PMCID:

PMC2876646.

48.

Talemi SR, Hofer T. Antiviral interferon response at single-cell resolution. Immunol Rev. 2018; 285

(1):72–80. https://doi.org/10.1111/imr.12699 PMID: 30129203.

49.

Kumar S, Morrison JH, Dingli D, Poeschla E. HIV-1 Activation of Innate Immunity Depends Strongly

on the Intracellular Level of TREX1 and Sensing of Incomplete Reverse Transcription Products. J

Virol. 2018;92(16). Epub 20180731. https://doi.org/10.1128/JVI.00001-18 PMID: 29769349; PubMed

Central PMCID: PMC6069178.

50.

Padmanabhan P, Garaigorta U, Dixit NM. Emergent properties of the interferon-signalling network

may underlie the success of hepatitis C treatment. Nat Commun. 2014; 5:3872. Epub 20140516.

https://doi.org/10.1038/ncomms4872 PMID: 24834957.

51.

Garaigorta U, Chisari FV. Hepatitis C virus blocks interferon effector function by inducing protein

kinase R phosphorylation. Cell Host Microbe. 2009; 6(6):513–22. https://doi.org/10.1016/j.chom.2009.

11.004 PMID: 20006840; PubMed Central PMCID: PMC2905238.

52.

Aso H, Ito J, Koyanagi Y, Sato K. Comparative description of the expression profile of interferon-stimulated genes in multiple cell lineages targeted by HIV-1 infection. Front Microbiol. 2019; 10:429. Epub

2019/03/28. https://doi.org/10.3389/fmicb.2019.00429 PMID: 30915053; PubMed Central PMCID:

PMC6423081.

53.

Hyrcza MD, Kovacs C, Loutfy M, Halpenny R, Heisler L, Yang S, et al. Distinct transcriptional profiles

in ex vivo CD4+ and CD8+ T cells are established early in human immunodeficiency virus type 1 infection and are characterized by a chronic interferon response as well as extensive transcriptional

changes in CD8+ T cells. J Virol. 2007; 81(7):3477–86. Epub 2007/01/26. https://doi.org/10.1128/JVI.

01552-06 PMID: 17251300; PubMed Central PMCID: PMC1866039.

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010053 April 25, 2022

24 / 27

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Antithetic effect of interferon-α on cell-free and cell-to-cell HIV-1 infection

54.

Sedaghat AR, German J, Teslovich TM, Cofrancesco J Jr., Jie CC, Talbot CC Jr., et al. Chronic CD4+

T-cell activation and depletion in human immunodeficiency virus type 1 infection: type I interferonmediated disruption of T-cell dynamics. J Virol. 2008; 82(4):1870–83. Epub 2007/12/14. https://doi.

org/10.1128/JVI.02228-07 PMID: 18077723; PubMed Central PMCID: PMC2258719.

55.

Xu X, Qiu C, Zhu L, Huang J, Li L, Fu W, et al. IFN-stimulated gene LY6E in monocytes regulates the

CD14/TLR4 pathway but inadequately restrains the hyperactivation of monocytes during chronic HIV1 infection. J Immunol. 2014; 193(8):4125–36. Epub 2014/09/17. https://doi.org/10.4049/jimmunol.

1401249 PMID: 25225669.

56.

Yu J, Liang C, Liu SL. CD4-Dependent Modulation of HIV-1 Entry by LY6E. J Virol. 2019; 93(7). Epub

2019/01/25. https://doi.org/10.1128/JVI.01866-18 PMID: 30674630; PubMed Central PMCID:

PMC6430548.

57.

Pfaender S, Mar KB, Michailidis E, Kratzel A, Boys IN, V’Kovski P, et al. LY6E impairs coronavirus

fusion and confers immune control of viral disease. Nat Microbiol. 2020;in press. Epub 2020/07/25.

https://doi.org/10.1038/s41564-020-0769-y PMID: 32704094.

58.

Agosto LM, Zhong P, Munro J, Mothes W. Highly active antiretroviral therapies are effective against

HIV-1 cell-to-cell transmission. PLoS Pathog. 2014; 10(2):e1003982. Epub 2014/03/04. https://doi.

org/10.1371/journal.ppat.1003982 PMID: 24586176; PubMed Central PMCID: PMC3937346.

59.

Duncan CJ, Russell RA, Sattentau QJ. High multiplicity HIV-1 cell-to-cell transmission from macrophages to CD4+ T cells limits antiretroviral efficacy. AIDS. 2013; 27(14):2201–6. Epub 2013/09/06.

https://doi.org/10.1097/QAD.0b013e3283632ec4 PMID: 24005480; PubMed Central PMCID:

PMC4714465.

60.

Sigal A, Kim JT, Balazs AB, Dekel E, Mayo A, Milo R, et al. Cell-to-cell spread of HIV permits ongoing

replication despite antiretroviral therapy. Nature. 2011; 477(7362):95–8. Epub 2011/08/19. https://doi.

org/10.1038/nature10347 PMID: 21849975.

61.

Best S, Le Tissier P, Towers G, Stoye JP. Positional cloning of the mouse retrovirus restriction gene

Fv1. Nature. 1996; 382(6594):826–9. Epub 1996/08/29. https://doi.org/10.1038/382826a0 PMID:

8752279.

62.

Pryciak PM, Varmus HE. Fv-1 restriction and its effects on murine leukemia virus integration in vivo

and in vitro. J Virol. 1992; 66(10):5959–66. Epub 1992/10/01. https://doi.org/10.1128/JVI.66.10.59595966.1992 PMID: 1326652; PubMed Central PMCID: PMC241473.

63.

Jimenez-Guardeno JM, Apolonia L, Betancor G, Malim MH. Immunoproteasome activation enables

human TRIM5α restriction of HIV-1. Nat Microbiol. 2019; 4(6):933–40. Epub 2019/03/20. https://doi.

org/10.1038/s41564-019-0402-0 PMID: 30886358; PubMed Central PMCID: PMC6544544.

64.

Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature. 2004; 427(6977):848–53.

Epub 2004/02/27. https://doi.org/10.1038/nature02343 PMID: 14985764.

65.

Passerini LD, Keckesova Z, Towers GJ. Retroviral restriction factors Fv1 and TRIM5α act independently and can compete for incoming virus before reverse transcription. J Virol. 2006; 80(5):2100–5.

Epub 2006/02/14. https://doi.org/10.1128/JVI.80.5.2100-2105.2006 PMID: 16474118; PubMed Central PMCID: PMC1395401.

66.

Shi J, Aiken C. Saturation of TRIM5α-mediated restriction of HIV-1 infection depends on the stability of

the incoming viral capsid. Virology. 2006; 350(2):493–500. Epub 2006/04/21. https://doi.org/10.1016/j.

virol.2006.03.013 PMID: 16624363.

67.

Sanz-Ramos M, Stoye JP. Capsid-binding retrovirus restriction factors: discovery, restriction specificity and implications for the development of novel therapeutics. J Gen Virol. 2013; 94(Pt 12):2587–98.

Epub 2013/09/13. https://doi.org/10.1099/vir.0.058180-0 PMID: 24026671.

68.

Sauter D, Kirchhoff F. IFITMs: Important Factors In Trans-Mission of HIV-1. Cell Host Microbe. 2016;

20(4):407–8. Epub 2016/10/14. https://doi.org/10.1016/j.chom.2016.09.009 PMID: 27736636.

69.

Yu J, Li M, Wilkins J, Ding S, Swartz TH, Esposito AM, et al. IFITM proteins restrict HIV-1 infection by

antagonizing the envelope glycoprotein. Cell Rep. 2015; 13(1):145–56. Epub 2015/09/22. https://doi.

org/10.1016/j.celrep.2015.08.055 PMID: 26387945; PubMed Central PMCID: PMC4602366.

70.

Tartour K, Appourchaux R, Gaillard J, Nguyen XN, Durand S, Turpin J, et al. IFITM proteins are incorporated onto HIV-1 virion particles and negatively imprint their infectivity. Retrovirology. 2014; 11:103.

Epub 2014/11/26. https://doi.org/10.1186/s12977-014-0103-y PMID: 25422070; PubMed Central

PMCID: PMC4251951.

71.

Cheney KM, McKnight A. Interferon-α mediates restriction of human immunodeficiency virus type-1

replication in primary human macrophages at an early stage of replication. PLoS One. 2010; 5(10):

e13521. Epub 2010/10/27. https://doi.org/10.1371/journal.pone.0013521 PMID: 20975956; PubMed

Central PMCID: PMC2958147.

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010053 April 25, 2022

25 / 27

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Antithetic effect of interferon-α on cell-free and cell-to-cell HIV-1 infection

72.

Sandler NG, Bosinger SE, Estes JD, Zhu RT, Tharp GK, Boritz E, et al. Type I interferon responses in

rhesus macaques prevent SIV infection and slow disease progression. Nature. 2014; 511(7511):601–

5. Epub 2014/07/22. https://doi.org/10.1038/nature13554 PMID: 25043006; PubMed Central PMCID:

PMC4418221.

73.

Yamada E, Nakaoka S, Klein L, Reith E, Langer S, Hopfensperger K, et al. Human-specific adaptations in Vpu conferring anti-tetherin activity are critical for efficient early HIV-1 replication in vivo. Cell

Host Microbe. 2018; 23(1):110–20 e7. https://doi.org/10.1016/j.chom.2017.12.009 PMID: 29324226.

74.

Cheng L, Yu H, Li G, Li F, Ma J, Li J, et al. Type I interferons suppress viral replication but contribute to

T cell depletion and dysfunction during chronic HIV-1 infection. JCI Insight. 2017; 2(12). Epub 2017/

06/15. https://doi.org/10.1172/jci.insight.94366 PMID: 28614789; PubMed Central PMCID:

PMC5470878.

75.

Law KM, Komarova NL, Yewdall AW, Lee RK, Herrera OL, Wodarz D, et al. In vivo HIV-1 cell-to-cell

transmission promotes multicopy micro-compartmentalized infection. Cell Rep. 2016; 15(12):2771–

83. Epub 2016/06/14. https://doi.org/10.1016/j.celrep.2016.05.059 PMID: 27292632.

76.

Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, von Andrian UH, et al. HIV-infected T

cells are migratory vehicles for viral dissemination. Nature. 2012; 490(7419):283–7. Epub 2012/08/03.

https://doi.org/10.1038/nature11398 PMID: 22854780; PubMed Central PMCID: PMC3470742.

77.

Ladinsky MS, Kieffer C, Olson G, Deruaz M, Vrbanac V, Tager AM, et al. Electron tomography of HIV1 infection in gut-associated lymphoid tissue. PLoS Pathog. 2014; 10(1):e1003899. Epub 2014/02/06.

https://doi.org/10.1371/journal.ppat.1003899 PMID: 24497830; PubMed Central PMCID:

PMC3907528.

78.

Real F, Sennepin A, Ganor Y, Schmitt A, Bomsel M. Live imaging of HIV-1 transfer across T cell virological synapse to epithelial cells that promotes stromal macrophage infection. Cell Rep. 2018; 23

(6):1794–805. Epub 2018/05/10. https://doi.org/10.1016/j.celrep.2018.04.028 PMID: 29742434.

79.

Dixit NM, Perelson AS. Multiplicity of human immunodeficiency virus infections in lymphoid tissue. J

Virol. 2004; 78(16):8942–5. Epub 2004/07/29. https://doi.org/10.1128/JVI.78.16.8942-8945.2004

PMID: 15280505; PubMed Central PMCID: PMC479058.

80.

Deleage C, Wietgrefe SW, Del Prete G, Morcock DR, Hao XP, Piatak M Jr., et al. Defining HIV and

SIV reservoirs in lymphoid tissues. Pathog Immun. 2016; 1(1):68–106. Epub 2016/07/19. https://doi.

org/10.20411/pai.v1i1.100 PMID: 27430032; PubMed Central PMCID: PMC4943335.

81.

Deleage C, Chan CN, Busman-Sahay K, Estes JD. Next-generation in situ hybridization approaches

to define and quantify HIV and SIV reservoirs in tissue microenvironments. Retrovirology. 2018; 15

(1):4. Epub 2018/01/11. https://doi.org/10.1186/s12977-017-0387-9 PMID: 29316956; PubMed Central PMCID: PMC5761108.

82.

Cavert W, Notermans DW, Staskus K, Wietgrefe SW, Zupancic M, Gebhard K, et al. Kinetics of

response in lymphoid tissues to antiretroviral therapy of HIV-1 infection. Science. 1997; 276

(5314):960–4. Epub 1997/05/09. https://doi.org/10.1126/science.276.5314.960 PMID: 9139661.

83.

Haase AT, Henry K, Zupancic M, Sedgewick G, Faust RA, Melroe H, et al. Quantitative image analysis

of HIV-1 infection in lymphoid tissue. Science. 1996; 274(5289):985–9. Epub 1996/11/08. https://doi.

org/10.1126/science.274.5289.985 PMID: 8875941.

84.

Dufloo J, Bruel T, Schwartz O. HIV-1 cell-to-cell transmission and broadly neutralizing antibodies. Retrovirology. 2018; 15(1):51. Epub 2018/07/30. https://doi.org/10.1186/s12977-018-0434-1 PMID:

30055632; PubMed Central PMCID: PMC6064125.

85.

Watanabe T, Urano E, Miyauchi K, Ichikawa R, Hamatake M, Misawa N, et al. The hematopoietic cellspecific Rho GTPase inhibitor ARHGDIB/D4GDI limits HIV type 1 replication. AIDS research and

human retroviruses. 2012; 28(8):913–22. Epub 2011/09/23. https://doi.org/10.1089/AID.2011.0180

PMID: 21936715.

86.

Ebina H, Kanemura Y, Misawa N, Sakuma T, Kobayashi T, Yamamoto T, et al. A high excision potential of TALENs for integrated DNA of HIV-based lentiviral vector. PLoS One. 2015; 10(3):e0120047.

Epub 2015/03/18. https://doi.org/10.1371/journal.pone.0120047 PMID: 25781496; PubMed Central

PMCID: PMC4363575.

87.

Ikeda T, Molan AM, Jarvis MC, Carpenter MA, Salamango DJ, Brown WL, et al. HIV-1 restriction by

endogenous APOBEC3G in the myeloid cell line THP-1. J Gen Virol. 2019; 100(7):1140–52. Epub

2019/05/31. https://doi.org/10.1099/jgv.0.001276 PMID: 31145054.

88.

Nakano Y, Yamamoto K, Ueda MT, Soper A, Konno Y, Kimura I, et al. A role for gorilla APOBEC3G in

shaping lentivirus evolution including transmission to humans. PLoS Pathog. 2020; 16(9):e1008812.

Epub 2020/09/12. https://doi.org/10.1371/journal.ppat.1008812 PMID: 32913367.

89.

Albin JS, Hache G, Hultquist JF, Brown WL, Harris RS. Long-term restriction by APOBEC3F selects

human immunodeficiency virus type 1 variants with restored Vif function. J Virol. 2010; 84(19):10209–

PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1010053 April 25, 2022

26 / 27

A Self-archived copy in

Kyoto University Research Information Repository

https://repository.kulib.kyoto-u.ac.jp

PLOS COMPUTATIONAL BIOLOGY

Antithetic effect of interferon-α on cell-free and cell-to-cell HIV-1 infection

19. Epub 2010/08/06. https://doi.org/10.1128/JVI.00632-10 PMID: 20686027; PubMed Central

PMCID: PMC2937771.

90.

Nakano Y, Misawa N, Juarez-Fernandez G, Moriwaki M, Nakaoka S, Funo T, et al. HIV-1 competition

experiments in humanized mice show that APOBEC3H imposes selective pressure and promotes

virus adaptation. PLoS Pathog. 2017; 13(5):e1006348. https://doi.org/10.1371/journal.ppat.1006348

PMID: 28475648; PubMed Central PMCID: PMC5435363.

91.

Sato K, Izumi T, Misawa N, Kobayashi T, Yamashita Y, Ohmichi M, et al. Remarkable lethal G-to-A

mutations in vif-proficient HIV-1 provirus by individual APOBEC3 proteins in humanized mice. Journal

of Virology. 2010; 84(18):9546–56. https://doi.org/10.1128/JVI.00823-10 PMID: 20610708.

92.

Sato K, Misawa N, Iwami S, Satou Y, Matsuoka M, Ishizaka Y, et al. HIV-1 Vpr accelerates viral replication during acute infection by exploitation of proliferating CD4+ T cells in vivo. PLoS Pathog. 2013; 9

(12):e1003812. Epub 2013/12/18. https://doi.org/10.1371/journal.ppat.1003812 PMID: 24339781;

PubMed Central PMCID: PMC3855622.

93.

Sato K, Takeuchi JS, Misawa N, Izumi T, Kobayashi T, Kimura Y, et al. APOBEC3D and APOBEC3F

potently promote HIV-1 diversification and evolution in humanized mouse model. PLoS Pathog. 2014;

10(10):e1004453. Epub 2014/10/21. https://doi.org/10.1371/journal.ppat.1004453 PMID: 25330146;

PubMed Central PMCID: PMC4199767.

94.

Freel SA, Picking RA, Ferrari G, Ding H, Ochsenbauer C, Kappes JC, et al. Initial HIV-1 antigen-specific CD8+ T cells in acute HIV-1 infection inhibit transmitted/founder virus replication. J Virol. 2012; 86

(12):6835–46. Epub 2012/04/20. https://doi.org/10.1128/JVI.00437-12 PMID: 22514337; PubMed

Central PMCID: PMC3393529.

95.

Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, Salazar MG, et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4

T lymphocytes and monocyte-derived macrophages. J Virol. 2012; 86(5):2715–28. Epub 2011/12/23.

https://doi.org/10.1128/JVI.06157-11 PMID: 22190722; PubMed Central PMCID: PMC3302286.

96.

Carlson LA, de Marco A, Oberwinkler H, Habermann A, Briggs JA, Krausslich HG, et al. Cryo electron

tomography of native HIV-1 budding sites. PLoS Pathog. 2010; 6(11):e1001173. Epub 2010/12/03.

https://doi.org/10.1371/journal.ppat.1001173 PMID: 21124872; PubMed Central PMCID:

PMC2991257.

97.

Briggs JA, Simon MN, Gross I, Krausslich HG, Fuller SD, Vogt VM, et al. The stoichiometry of Gag protein in HIV-1. Nat Struct Mol Biol. 2004; 11(7):672–5. Epub 2004/06/23. https://doi.org/10.1038/

nsmb785 PMID: 15208690.

98.

Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. Development of a self-inactivating lentivirus

vector. J Virol. 1998; 72(10):8150–7. Epub 1998/09/12. PubMed Central PMCID: PMC110156. https://

doi.org/10.1128/JVI.72.10.8150-8157.1998 PMID: 9733856

99.

Richardson RB, Ohlson MB, Eitson JL, Kumar A, McDougal MB, Boys IN, et al. A CRISPR screen

identifies IFI6 as an ER-resident interferon effector that blocks flavivirus replication. Nat Microbiol.

2018; 3(11):1214–23. Epub 2018/09/19. https://doi.org/10.1038/s41564-018-0244-1 PMID:

30224801; PubMed Central PMCID: PMC6202210.

100.

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14(4):R36.

Epub 2013/04/27. https://doi.org/10.1186/gb-2013-14-4-r36 PMID: 23618408; PubMed Central

PMCID: PMC4053844.

101.

Love MI, Huber W, ...