Efficiency of cell-free and cell-associated virus in mucosal transmission of human immunodeficiency virus type 1 and simian immunodeficiency virus

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13589-13597

  Kolodkin Gal, Dror ^a,b   Hulot, Sandrine L ^a   Korioth Schmitz, Birgit ^a   Gombos, Randi B ^a   Zheng, Yi ^a   Owuor, Joshua ^a   Lifton, Michelle A ^a   Ayeni, Christian ^a   Najarian, Robert M ^a   Yeh, Wendy W ^a   Asmal, Mohammed ^a   Zamir, Gideon ^b   Letvin, Norman L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA; VIRUS RNA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL FREE SYSTEM; COLON BIOPSY; COLON MUCOSA; CONTROLLED STUDY; EX VIVO STUDY; EXPLANT; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; IN VIVO STUDY; LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RHESUS MONKEY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS LOAD; VIRUS PATHOGENESIS; VIRUS TRANSMISSION;

ANIMALS; COLON; HIV INFECTIONS; HIV-1; HUMANS; INTESTINAL MUCOSA; MACACA MULATTA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84888048483     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03108-12     Document Type: Article

References (36)

1. Anderson DJ, Yunis EJ. 1983. "Trojan horse" leukocytes in AIDS. N. Engl. J. Med. 309:984-985.
2. Kashuba AD, Dyer JR, Kramer LM, Raasch RH, Eron JJ, Cohen MS. 1999. Antiretroviral-drug concentrations in semen:implications for sexual transmission of human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 43:1817-1826.
3. Virgin HW, Walker BD. 2010. Immunology and the elusive AIDS vaccine. Nature 464:224-231.
4. Vernazza PL. 2005. HIV in semen:still more to be learned. AIDS Res. Ther. 2:11. doi:10.1186/1742-6405-2-11.
5. Letvin NL. 2008. Immunology of HIV infection, p 1204-1232. In Paul WE (ed), Fundamental immunology, 6th ed. Wolter Kluwer/Lippincott, Williams & Wilkins, Philadelphia, PA.
6. Abela IA, Berlinger L, Schanz M, Reynell L, Gunthard HF, Rusert P, Trkola A. 2012. Cell-cell transmission enables HIV-1 to evade inhibition by potent CD4bs directed antibodies. PLoS Pathog. 8:e1002634. doi:10.1371/journal.ppat.1002634.
7. Ferrari G, Pollara J, Kozink D, Harms T, Drinker M, Freel S, Moody MA, Alam SM, Tomaras GD, Ochsenbauer C, Kappes JC, Shaw GM, Hoxie JA, Robinson JE, Haynes BF. 2011. An HIV-1 gp120 envelope human monoclonal antibody that recognizes a C1 conformational epitope mediates potent antibody-dependent cellular cytotoxicity (ADCC) activity and defines a common ADCC epitope in human HIV-1 serum. J. Virol. 85:7029-7036.
8. Ancuta P, Autissier P, Wurcel A, Zaman T, Stone D, Gabuzda D. 2006. CD16+ monocyte-derived macrophages activate resting T cells for HIV infection by producing CCR3 and CCR4 ligands. J. Immunol. 176:5760-5771.
9. Liu J, Keele BF, Li H, Keating S, Norris PJ, Carville A, Mansfield KG, Tomaras GD, Haynes BF, Kolodkin-Gal D, Letvin NL, Hahn BH, Shaw GM, Barouch DH. 2010. Low-dose mucosal simian immunodeficiency virus infection restricts early replication kinetics and transmitted virus variants in rhesus monkeys. J. Virol. 84:10406-10412.
10. Vacharaksa A, Asrani AC, Gebhard KH, Fasching CE, Giacaman RA, Janoff EN, Ross KF, Herzberg MC. 2008. Oral keratinocytes support non-replicative infection and transfer of harbored HIV-1 to permissive cells. Retrovirology 5:66. doi:10.1186/1742-4690-5-66.
11. Finney DJ. 1978. Statistical method in biological assay, 3rd ed, vol 3. Charles Griffin & Co. Ltd., London, United Kingdom.
12. Kolodkin-Gal D, Zamir G, Edden Y, Pikarsky E, Pikarsky A, Haim H, Haviv YS, Panet A. 2008. Herpes simplex virus type 1 preferentially targets human colon carcinoma:role of extracellular matrix. J. Virol. 82:999-1010.
13. Massler A, Kolodkin-Gal D, Meir K, Khalaileh A, Falk H, Izhar U, Shufaro Y, Panet A. 2011. Infant lungs are preferentially infected by adenovirus and herpes simplex virus type 1 vectors:role of the tissue mesenchymal cells. J. Gene Med. 13:101-113.
14. Salle B, Brochard P, Bourry O, Mannioui A, Andrieu T, Prevot S, Dejucq-Rainsford N, Dereuddre-Bosquet N, Le Grand R. 2010. Infection of macaques after vaginal exposure to cell-associated simian immunodeficiency virus. J. Infect. Dis. 202:337-344.
15. Politch JA, Mayer KH, Anderson DJ. 2009. Depletion of CD4+ T cells in semen during HIV infection and their restoration following antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 50:283-289.
16. Anderson DJ, Politch JA, Nadolski AM, Blaskewicz CD, Pudney J, Mayer KH. 2010. Targeting Trojan horse leukocytes for HIV prevention. AIDS 24:163-187.
17. Cline AN, Bess JW, Piatak M, Jr, Lifson JD. 2005. Highly sensitive SIV plasma viral load assay:practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J. Med. Primatol. 34:303-312.
18. Nishimura Y, Sadjadpour R, Mattapallil JJ, Igarashi T, Lee W, Buckler-White A, Roederer M, Chun TW, Martin MA. 2009. High frequencies of resting CD4+T cells containing integrated viral DNA are found in rhesus macaques during acute lentivirus infections. Proc. Natl. Acad. Sci. U.S.A. 106:8015-8020.
19. Collins KB, Patterson BK, Naus GJ, Landers DV, Gupta P. 2000. Development of an in vitro organ culture model to study transmission of HIV-1 in the female genital tract. Nat. Med. 6:475-479.
20. Mayer KH, Boswell S, Goldstein R, Lo W, Xu C, Tucker L, DePasquale MP, D'Aquila R, Anderson DJ. 1999. Persistence of human immunodeficiency virus in semen after adding indinavir to combination antiretroviral therapy. Clin. Infect. Dis. 28:1252-1259.
21. Mahalingam A, Jay JI, Langheinrich K, Shukair S, McRaven MD, Rohan LC, Herold BC, Hope TJ, Kiser PF. 2011. Inhibition of the transport of HIV in vitro using a pH-responsive synthetic mucin-like polymer system. Biomaterials 32:8343-8355.
22. Habte HH, de Beer C, Lotz ZE, Roux P, Mall AS. 2010. Anti-HIV-1 activity of salivary MUC5B and MUC7 mucins from HIV patients with different CD4 counts. Virol. J. 7:269.
23. Gali Y, Arien KK, Praet M, Van den Bergh R, Temmerman M, Delezay O, Vanham G. 2010. Development of an in vitro dual-chamber model of the female genital tract as a screening tool for epithelial toxicity. J. Virol. Methods 165:186-197.
24. Lawrence P, Portran D, Terrasse R, Palle S, Olivier T, Fantini J, Bourlet T, Pozzetto B, Delezay O. 2012. Selective transmigration of monocyteassociated HIV-1 across a human cervical monolayer and its modulation by seminal plasma. AIDS 26:785-796.
25. Khanna KV, Whaley KJ, Zeitlin L, Moench TR, Mehrazar K, Cone RA, Liao Z, Hildreth JE, Hoen TE, Shultz L, Markham RB. 2002. Vaginal transmission of cell-associated HIV-1 in the mouse is blocked by a topical, membrane-modifying agent. J. Clin. Invest. 109:205-211.
26. Ibata B, Parr EL, King NJ, Parr MB. 1997. Migration of foreign lymphocytes from the mouse vagina into the cervicovaginal mucosa and to the iliac lymph nodes. Biol. Reprod. 56:537-543.
27. Jung A, Maier R, Vartanian JP, Bocharov G, Jung V, Fischer U, Meese E, Wain-Hobson S, Meyerhans A. 2002. Recombination:multiply infected spleen cells in HIV patients. Nature 418:144.
28. Wolff H, Anderson DJ. 1988. Immunohistologic characterization and quantitation of leukocyte subpopulations in human semen. Fertil. Steril. 49:497-504.
29. Keele BF, Li H, Learn GH, Hraber P, Giorgi EE, Grayson T, Sun C, Chen Y, Yeh WW, Letvin NL, Mascola JR, Nabel GJ, Haynes BF, Bhattacharya T, Perelson AS, Korber BT, Hahn BH, Shaw GM. 2009. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J. Exp. Med. 206:1117-1134.
30. Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, Lynch DM, Iampietro MJ, SanMiguel A, Seaman MS, Ferrari G, Forthal DN, Ourmanov I, Hirsch VM, Carville A, Mansfield KG, Stablein D, Pau MG, Schuitemaker H, Sadoff JC, Billings EA, Rao M, Robb ML, Kim JH, Marovich MA, Goudsmit J, Michael NL. 2012. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 482:89-93.
31. Stekler J, Sycks BJ, Holte S, Maenza J, Stevens CE, Dragavon J, Collier AC, Coombs RW. 2008. HIV dynamics in seminal plasma during primary HIV infection. AIDS Res. Hum. Retroviruses 24:1269-1274.
32. Sodora DL, Gettie A, Miller CJ, Marx PA. 1998. Vaginal transmission of SIV:assessing infectivity and hormonal influences in macaques inoculated with cell-free and cell-associated viral stocks. AIDS Res. Hum. Retroviruses 14(Suppl 1):S119-S123.
33. Nobile C, Rudnicka D, Hasan M, Aulner N, Porrot F, Machu C, Renaud O, Prevost MC, Hivroz C, Schwartz O, Sol-Foulon N. 2010. HIV-1 Nef inhibits ruffles, induces filopodia, and modulates migration of infected lymphocytes. J. Virol. 84:2282-2293.
34. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, Kohler K, Oddos S, Eissmann P, Brodsky FM, Hopkins C, Onfelt B, Sattentau Q, Davis DM. 2008. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10:211-219.
35. Sattentau Q. 2008. Avoiding the void:cell-to-cell spread of human viruses. Nat. Rev. Microbiol. 6:815-826.
36. Sigal A, Kim JT, Balazs AB, Dekel E, Mayo A, Milo R, Baltimore D. 2011. Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy. Nature 477:95-98.