On the efficiency of HIV transmission: Insights through discrete time HIV models

English version

Autoři: Sarudzai P. Showa ^aff001; Farai Nyabadza ^aff002; Senelani D. Hove-Musekwa ^aff001
Působiště autorů: Department of Applied Mathematics, National University of Science and Technology, Bulawayo, Zimbabwe ^aff001; Department of Mathematics and Applied Mathematics, Auckland Park Campus, University of Johannesburg, Johannesburg, South Africa ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222574

Souhrn

There are different views on which of the two forms of viral spread is more efficient in vivo between cell-free and cell-associated virus. In this study, discrete time human immunodeficiency virus models are formulated and analysed with the goal of determining the form of viral spread that is more efficient in vivo. It is shown that on its own, cell-free viral spread cannot sustain an infection owing to the low infectivity of cell-free virus and cell-associated virus can sustain an infection because of the high infectivity of cell-associated virus. When acting concurrently, cell-associated virus is more efficient in spreading the infection upon exposure to the virus. However, in the long term, the two forms of viral spread contribute almost equally. Both forms of viral spread are shown to be able to initiate an infection.

Klíčová slova:

Biology and life sciences – Cell biology – Organisms – Developmental biology – Cellular types – Animal cells – Anatomy – Medicine and health sciences – Microbiology – Medical microbiology – Microbial pathogens – Pathology and laboratory medicine – Pathogens – Physiology – Infectious diseases – Viral pathogens – Immunodeficiency viruses – HIV – Retroviruses – Lentivirus – Viruses – RNA viruses – Immunology – Body fluids – Blood – Virology – Blood cells – White blood cells – T cells – Immune cells – Viral diseases – HIV infections – Sexually transmitted diseases – Life cycles – Viral structure – Virions – Semen

Zdroje

1. Hübner W, McNerney GP, Chen P, Dale BM, Gordon RE, Chuang FYS, et al. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science. 2009;323: 1743–1747. doi: 10.1126/science.1167525 19325119

2. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O. Inefficient Human Immunodeficiency Virus replication in mobile lymphocytes. J. Virol. 2007;81(2): 1000–1012. doi: 10.1128/JVI.01629-06 17079292

3. Barreto-de-Souza V, Arakelyan A, Margolis L, Vanpouille C. HIV-1 vaginal transmission: cell-free or cell-associated virus? Am. J. Reprod. Immunol. 2014;71: 589–599. doi: 10.1111/aji.12240 24730358

4. Sagar M. Origin of the transmitted virus in HIV infection: Infected cells versus cell-free virus. J. Infect. Dis.2014;210(3): S667–S673 doi: 10.1093/infdis/jiu369 25414422

5. Anderson DJ, Politch JA, Nadolski AM, Blaskewicz CD, Pudney J, Mayer KH. Targeting Trojan Horse leukocytes for HIV prevention. AIDS. 2010;24: 163–187. doi: 10.1097/QAD.0b013e32833424c8 20010071

6. Sato H, Orestein J, Dimitrov D, Martin M. Cell to cell spread of HIV occurs within minutes and may not involve virus particles. Virology. 1992;186: 712–724.

7. Mothes W, Sherer NM, Jin J, Zhong P. Virus cell-to-cell transmission. J. Virol. 2010;84(17): 8360–8368. doi: 10.1128/JVI.00443-10 20375157

8. Car JM, Hocking H, Li P, Burrel C. Rapid and efficient cell-to-cell transmission of human immunodeficiency virus infection from monocyte-derived macrophages to peripheral blood lymphocytes. Virology. 1999;265: 319–329. doi: 10.1006/viro.1999.0047

9. Heath L, Frenkel LM, Foley BT, Mullins JI. Comment on “The origins of sexually transmitted HIV among men who have sex with men”. Sci. Transl. Med. 2010;2(5): 50le1. doi: 10.1126/scitranslmed.3001416 20861507

10. Zhu T, Wang N, Carr A, Nam DS, Moor-Jankowski R, Cooper DA, et al. Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: evidence for viral compartmentalization and selection during sexual transmission. J. Virol. 1996;70: 3098–3107.

11. Peters B, Whittall T, Babaahmady K, Gray K, Vaughan R, Lehner T. Effect of heterosexual intercourse on mucosal alloimmunisation and resistance to HIV-1 infection. Lancet. 2004;363: 518–524. doi: 10.1016/S0140-6736(04)15538-4 14975614

12. Butler DM, Delport W, Kosakovsky SL, Pond M, Lakdawala K, Cheng PM, et al. The origins of sexually transmitted HIV among men who have sex with men. Sci. Transl. Med. 2010;2: 18re1. doi: 10.1126/scitranslmed.3000447 20371483

13. Virgin HW, Walker BD. Immunology and the elusive AIDS vaccine. Nature. 2010;434: 224–231. doi: 10.1038/nature08898

14. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, et al. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N. Engl. J. Med. 2000;342: 921–929. doi: 10.1056/NEJM200003303421303 10738050

15. Butler DM, Smith DM, Cachay ER, Hightower GK, Nugent C, Richman DD, et al. Herpes simplex virus 2 serostatus and viral loads of HIV-1 in blood and semen as risk factors for HIV transmission among men who have sex with men. AIDS. 2008;22: 1667–1671. doi: 10.1097/QAD.0b013e32830bfed8 18670228

16. Sturmer M, Doerr HW, Berger A, Gute P. Is transmission of HIV-1 in non-viraemic serodiscordant couples possible? Antivir. Ther. 2008;13: 729–732.

17. Rousseau CM, Nduati RW, Richardson BA, John-Stewart GC, Mbori-Ngacha DA, Kreiss JK, et al. Association of levels of HIV-1 infected breast milk cells and risk of mother-to-child transmission. J. Infect. Dis. 2004;190: 1880–1888. doi: 10.1086/425076 15499546

18. Boeras DI, Hraber PT, Hurlston M, Evans-Strickfaden T, Bhattacharya T, Giorgi EE, et al. Role of donor genital tract HIV-1 diversity in the transmission bottleneck. Proc. Natl. Acad. Sci. U. S. A. 2011;108(46): E1156–E1163. doi: 10.1073/pnas.1103764108 22065783

19. Gianella S, Mehta SR, Young JA, Vargas MV, Little SJ, Richman DD, et al. Sexual transmission of predicted CXCR4-tropic HIV-1 likely originating from the source partner’s seminal cells. Virology. 2012;434: 2–4. doi: 10.1016/j.virol.2012.09.010 23040890

20. Frange P, Meyer L, Jung M, Goujard C, Zucman D, Abel S, et al. Sexually-transmitted/founder HIV-1 cannot be directly predicted from plasma or PBMC-derived viral quasispecies in the transmitting partner. PLoS ONE. 2013;8: e69144. doi: 10.1371/journal.pone.0069144 23874894

21. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD. HIV-1 dynamics in vivo: Virion clearance rate, infected cell life span and viral generation time. Science. 1996;271:1582–1586. doi: 10.1126/science.271.5255.1582 8599114

22. Srivastava PK, Banerjee M, Chandra P. A primary infection model for HIV and immune response with two Discrete time delays. Differ. Equ. and Dyn. Syst. 2010;18(4): 385–399. doi: 10.1007/s12591-010-0074-y

23. Srivastava PK, Chandra P. Modelling the Dynamics of HIV and CD4+T Cells during primary infection. Nonlinear Anal. Real World Appl. 2010;11(2): 612–618. doi: 10.1016/j.nonrwa.2008.10.037

24. Wang SF, Zou DY, Global stability of in-host viral models with humoral immunity and intracellular delays. Appl. Math. Model. 2012;36:1313–1322. doi: 10.1016/j.apm.2011.07.086

25. Lai X, Zou X. Modeling HIV-1 virus dynamics with both virus-to-cell infection and cell-to-cell transmission. SIAM J. Appl. Math. 2014;74: 898–917. doi: 10.1137/130930145

26. Wang J, Guo M, Liu X, Zhao Z. Threshold dynamics of HIV-1 virus model with cell-to-cell transmission, cell-mediated immune responses and distributed delay. Appl. Math. Comput. 2016;291: 49–161.

27. Elaiw AM, Raezah AA, Alofi AS. Effect of humoral immunity on HIV-1 dynamics with virus-to-target and infected-to-target infections. AIP Adv. 2016;6: 085204 doi: 10.1063/1.4960987

28. Lin J, Xu R, Tian X. Threshold dynamics of an HIV-1 virus model with both virus-to-cell and cell-to-cell transmissions, intracellular delay, and humoral immunity. Appl. Math. Comput. 2017;315: 516–530.

29. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 1993;67(4): 2182–2190. 8445728

30. Komarova NL, Anghelina D, Voznesensky I, Trinitè B, Levy DN, Wodarz D. Relative contribution of free-virus and synaptic transmission to the spread of HIV-1 through target cell populations. Biol. Lett. 2013;9. doi: 10.1098/rsbl.2012.1049 23269844

31. Iwami S, Takeuchi JS, Nakaoka S, Nakaoka SM, Cell-to-cell infection by HIV contributes over half of virus infection. Elife. 2015;6(4).

32. Powers KA, Poole C, Pettifor AE, Cohen MS. Rethinking the heterosexual infectivity of HIV-1: a systematic review and meta-analysis. Lancet Infect. Dis. 2008;8: 553–563. doi: 10.1016/S1473-3099(08)70156-7 18684670

33. Kirschner D. Using Mathematics to understand HIV immune dynamics. Not. Am. Math. Soc. 1996;43(2): 193–202.

34. Bangham CR. The immune control and cell-to-cell spread of human T-lymphotropic irus type 1. J. Gen. Virol. 2003;84: 3177–3189. doi: 10.1099/vir.0.19334-0 14645900

35. Gupta P, Balachandran R, Ho M, Enrico A, Rinaldo C. Cell-to-cell transmission of human immmuno deficiency virus type 1 in the presence of azidothymidine and neutralizing antibodies. J. Virol. 1989;63: 2361–2365. 2704079

36. Sedhagat AR, Dinoso JB, Shen L, Wilke CO, Siliciano RF. Decay dynamics of HIV-1 depend on the inhibited stages of the viral life cycle. Proc. Natl. Acad. Sci. U. S. A. 2008;105(12): 4832–4837. doi: 10.1073/pnas.0711372105

37. Showa SP, Nyabadza F, Hove-Musekwa SD. A discrete HIV infection model with immunosenescence. Biol. Med. 2017;9: 420.

38. Sedhaghat AR, Siliciano RF, Wilke CO. Constraints on the dominant mechanism for HIV viral dynamics in patients on raltegraviar. Antivir. Ther. 2009;14: 263–261.

39. von Kleist M, Menz S, Huisinga W. Drug-Class specific impact of antivirals on the reproductive capacity of HIV. PLoS Comput. Biol. 2010;6(3): e1000720. doi: 10.1371/journal.pcbi.1000720 20361047

40. Anderson JD. Finally, a Macaque Model for Cell-Associated SIV/HIV Vaginal Transmission. J. Infect. Dis. 2010;202(3): 333–336. doi: 10.1086/653620 20569159

41. Kolodkin-Gal D, Hulot SL, Korioth-Schmitz B, Gombos RB, Zheng Y, Owuor J, et al. Efficiency of cell-free and cell-associated virus in mucosal transmission of human immunodeficiency virus type 1 and simian immunodeficiency virus. J. Virol. 2013;7(24): 13589–13597. doi: 10.1128/JVI.03108-12

42. Abela IA, Berlinger L, Schanz M, Reynell L, Gunthard H F, Rusert P, et al. Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies. PLoS Pathog. 2012;8(4): e1002634. doi: 10.1371/journal.ppat.1002634 22496655

43. Pantaleo G, Graziosi C, Demarest JF, Butini L, Montroni M, Fox CH, et al. HIV infection is active and progressive in lymphoid tissue during clinically latent stage of disease Nature 1998 362: 341–345.

44. Embretson J, Zupancicl M, Ribas JL. Massive convert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS Nature 1992;362: 359–362. doi: 10.1038/362359a0

45. Westermann J, Pabst R. Lymphocyte subsets in the blood, a diagonistic window on the lymphoid system. Immunol. Today 1990;11: 406–410. doi: 10.1016/0167-5699(90)90160-B 2078294

46. Rosenberg YJ, Janossy G. The importance of lymphocyte trafficking in regulating blood lymphocyte levels during HIV and SIV infections Sem. Immunol. 1999;11(2):139–54.

47. Krämer A Kretzschmar M, Krickrberg K. (eds.) Modern infectious disease epidemiology: Concepts, methods, mathematical models and public health (Statistics for biology and health). Springer Science Business Media, LLC 2010.

48. Showa SP, Nyabadza F, Hove-Musekwa SD, Magombedze G. A comparison of elasticities of viral levels to specific immune response mechanisms in human immunodeficiency virus infection. BMC Res. Notes 2014;7: 37. doi: 10.1186/1756-0500-7-737

49. Zack JA, Arrigo SJ, Weitsman SR, Go ASA, Haislip A, Chen ISY. HIV-1 entry into quiescent primary lymphocytes: Molecular analysis reveals a labile, latent viral structure. Cell 1990;61(2): 213–222. doi: 10.1016/0092-8674(90)90802-l 2331748

50. Zack JA, Haislip AM, Krogstand P, Chen ISY. Incompletely reverse-transcribed human immunodeficiency virus type I genomes function as intermediates in the retroviral life cycle. J. Virol. 1992;66: 1717–1725.

51. Barbosa P, Charneau D, Durney N, Clavel F. Kinetic Analysis of HIV-1 early replicative steps in a coculture. AIDS Res. Hum. Retroviruses. 1994;10(1): 53–59. doi: 10.1089/aid.1994.10.53 8179964

52. Brinchmann JE, Albert J, Vartal F. Few infected CD4+T cells but a high proportion of replication-competent provirus in the asymptomatic human immunodefiency virus type 1 infection. J. Virol. 1991;65(4): 2019–2023. 1672165

53. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 1993;67(4): 2182–2190. 8445728

On the efficiency of HIV transmission: Insights through discrete time HIV models

Souhrn

Klíčová slova:

Zdroje

PLOS One

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Eozinofilní granulomatóza s polyangiitidou