Tissue myeloid cells in SIV-infected primates acquire viral DNA through phagocytosis of infected T cells

Immunity

Volumn 41, Issue 3, 2014, Pages 493-502

  Calantone, Nina ^a   Wu, Fan ^a   Klase, Zachary ^a   Deleage, Claire ^b   Perkins, Molly ^a   Matsuda, Kenta ^a   Thompson, Elizabeth A ^a,c   Ortiz, Alexandra M ^a   Vinton, Carol L ^a   Ourmanov, Ilnour ^a   Loré, Karin ^a,c   Douek, Daniel C ^a   Estes, Jacob D ^b   Hirsch, Vanessa M ^a   Brenchley, Jason M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; VIRUS PROTEIN; VPX PROTEIN, SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CELL PHAGOCYTOSIS; CHLOROCEBUS AETHIOPS; IN VITRO STUDY; IN VIVO STUDY; MACACA; NONHUMAN; PROTEIN EXPRESSION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; T CELL DEPLETION; TARGET CELL; VIRUS LOAD; ANIMAL; BIOSYNTHESIS; GENETICS; IMMUNOLOGY; LYMPHOCYTE DEPLETION; PHAGOCYTOSIS; SIMIAN IMMUNODEFICIENCY VIRUS; VIROLOGY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CERCOPITHECUS AETHIOPS; DNA, VIRAL; LYMPHOCYTE DEPLETION; MACACA; MONOMERIC GTP-BINDING PROTEINS; MYELOID CELLS; PHAGOCYTOSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84907996442     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2014.08.014     Document Type: Article

References (49)

1. Alexaki A., Liu Y., Wigdahl B. Cellular reservoirs of HIV-1 and their role in viral persistence. Curr. HIV Res. 2008, 6:388-400.
2. Baldauf H.M., Pan X., Erikson E., Schmidt S., Daddacha W., Burggraf M., Schenkova K., Ambiel I., Wabnitz G., Gramberg T., et al. SAMHD1 restricts HIV-1 infection in resting CD4(+) Tcells. Nat. Med. 2012, 18:1682-1687.
3. Berger A., Sommer A.F., Zwarg J., Hamdorf M., Welzel K., Esly N., Panitz S., Reuter A., Ramos I., Jatiani A., et al. SAMHD1-deficient CD14+ cells from individuals with Aicardi-Goutières syndrome are highly susceptible to HIV-1 infection. PLoS Pathog. 2011, 7:e1002425.
4. Berger G., Turpin J., Cordeil S., Tartour K., Nguyen X.N., Mahieux R., Cimarelli A. Functional analysis of the relationship between Vpx and the restriction factor SAMHD1. J.Biol. Chem. 2012, 287:41210-41217.
5. Bloch N., O'Brien M., Norton T.D., Polsky S.B., Bhardwaj N., Landau N.R. HIV type 1 infection of plasmacytoid and myeloid dendritic cells is restricted by high levels of SAMHD1 and cannot be counteracted by Vpx. AIDS Res. Hum. Retroviruses 2014, 30:195-203.
6. Brenchley J.M., Hill B.J., Ambrozak D.R., Price D.A., Guenaga F.J., Casazza J.P., Kuruppu J., Yazdani J., Migueles S.A., Connors M., et al. T-cell subsets that harbor human immunodeficiency virus (HIV) invivo: implications for HIV pathogenesis. J.Virol. 2004, 78:1160-1168.
7. Brenchley J.M., Schacker T.W., Ruff L.E., Price D.A., Taylor J.H., Beilman G.J., Nguyen P.L., Khoruts A., Larson M., Haase A.T., Douek D.C. CD4+ Tcell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J.Exp. Med. 2004, 200:749-759.
8. Burdo T.H., Soulas C., Orzechowski K., Button J., Krishnan A., Sugimoto C., Alvarez X., Kuroda M.J., Williams K.C. Increased monocyte turnover from bone marrow correlates with severity of SIV encephalitis and CD163 levels in plasma. PLoS Pathog. 2010, 6:e1000842.
9. Cline A.N., Bess J.W., Piatak M., Lifson J.D. Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J.Med. Primatol. 2005, 34:303-312.
10. Combadiere B., Boissonnas A., Carcelain G., Lefranc E., Samri A., Bricaire F., Debre P., Autran B. Distinct time effects of vaccination on long-term proliferative and IFN-gamma-producing Tcell memory to smallpox in humans. J.Exp. Med. 2004, 199:1585-1593.
11. Cribier A., Descours B., Valadão A.L., Laguette N., Benkirane M. Phosphorylation of SAMHD1 by cyclin A2/CDK1 regulates its restriction activity toward HIV-1. Cell Rep 2013, 3:1036-1043.
12. Dai L., Lidie K.B., Chen Q., Adelsberger J.W., Zheng X., Huang D., Yang J., Lempicki R.A., Rehman T., Dewar R.L., et al. IL-27 inhibits HIV-1 infection in human macrophages by down-regulating host factor SPTBN1 during monocyte to macrophage differentiation. J.Exp. Med. 2013, 210:517-534.
13. Dang Q., Whitted S., Goeken R.M., Brenchley J.M., Matsuda K., Brown C.R., Lafont B.A., Starost M.F., Iyengar R., Plishka R.J., et al. Development of neurological disease is associated with increased immune activation in simian immunodeficiency virus-infected macaques. J.Virol. 2012, 86:13795-13799.
14. Descours B., Cribier A., Chable-Bessia C., Ayinde D., Rice G., Crow Y., Yatim A., Schwartz O., Laguette N., Benkirane M. SAMHD1 restricts HIV-1 reverse transcription in quiescent CD4(+) T-cells. Retrovirology 2012, 9:87.
15. Finzi D., Blankson J., Siliciano J.D., Margolick J.B., Chadwick K., Pierson T., Smith K., Lisziewicz J., Lori F., Flexner C., et al. Latent infection of CD4+ Tcells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat. Med. 1999, 5:512-517.
16. Fregoso O.I., Ahn J., Wang C., Mehrens J., Skowronski J., Emerman M. Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog. 2013, 9:e1003496.
17. Gibbs J.S., Lackner A.A., Lang S.M., Simon M.A., Sehgal P.K., Daniel M.D., Desrosiers R.C. Progression to AIDS in the absence of a gene for vpr or vpx. J.Virol. 1995, 69:2378-2383.
18. Goldstone D.C., Ennis-Adeniran V., Hedden J.J., Groom H.C., Rice G.I., Christodoulou E., Walker P.A., Kelly G., Haire L.F., Yap M.W., et al. HIV-1 restriction factor SAMHD1 is a deoxynucleoside triphosphate triphosphohydrolase. Nature 2011, 480:379-382.
19. Gonzalez-Mejia M.E., Doseff A.I. Regulation of monocytes and macrophages cell fate. Front Biosci (Landmark Ed) 2009, 14:2413-2431.
20. Gonzalez-Perez M.P., O'Connell O., Lin R., Sullivan W.M., Bell J., Simmonds P., Clapham P.R. Independent evolution of macrophage-tropism and increased charge between HIV-1 R5 envelopes present in brain and immune tissue. Retrovirology 2012, 9:20.
21. Greter M., Merad M. Regulation of microglia development and homeostasis. Glia 2013, 61:121-127.
22. Heeregrave E.J., Geels M.J., Brenchley J.M., Baan E., Ambrozak D.R., van der Sluis R.M., Bennemeer R., Douek D.C., Goudsmit J., Pollakis G., et al. Lack of invivo compartmentalization among HIV-1 infected naïve and memory CD4+ Tcell subsets. Virology 2009, 393:24-32.
23. Hirsch V.M., Sharkey M.E., Brown C.R., Brichacek B., Goldstein S., Wakefield J., Byrum R., Elkins W.R., Hahn B.H., Lifson J.D., Stevenson M. Vpx is required for dissemination and pathogenesis of SIV(SM) PBj: evidence of macrophage-dependent viral amplification. Nat. Med. 1998, 4:1401-1408.
24. Hrecka K., Hao C., Gierszewska M., Swanson S.K., Kesik-Brodacka M., Srivastava S., Florens L., Washburn M.P., Skowronski J. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011, 474:658-661.
25. Igarashi T., Brown C.R., Endo Y., Buckler-White A., Plishka R., Bischofberger N., Hirsch V., Martin M.A. Macrophage are the principal reservoir and sustain high virus loads in rhesus macaques after the depletion of CD4+ Tcells by a highly pathogenic simian immunodeficiency virus/HIV type 1 chimera (SHIV): Implications for HIV-1 infections of humans. Proc. Natl. Acad. Sci. USA 2001, 98:658-663.
26. Igarashi T., Imamichi H., Brown C.R., Hirsch V.M., Martin M.A. The emergence and characterization of macrophage-tropic SIV/HIV chimeric viruses (SHIVs) present in CD4+ Tcell-depleted rhesus monkeys. J.Leukoc. Biol. 2003, 74:772-780.
27. Jenkins S.J., Ruckerl D., Cook P.C., Jones L.H., Finkelman F.D., van Rooijen N., MacDonald A.S., Allen J.E. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011, 332:1284-1288.
28. Katlama C., Deeks S.G., Autran B., Martinez-Picado J., van Lunzen J., Rouzioux C., Miller M., Vella S., Schmitz J.E., Ahlers J., et al. Barriers to a cure for HIV: new ways to target and eradicate HIV-1 reservoirs. Lancet 2013, 381:2109-2117.
29. Koenig S., Gendelman H.E., Orenstein J.M., Dal Canto M.C., Pezeshkpour G.H., Yungbluth M., Janotta F., Aksamit A., Martin M.A., Fauci A.S. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 1986, 233:1089-1093.
30. Koppensteiner H., Brack-Werner R., Schindler M. Macrophages and their relevance in human immunodeficiency virus type I infection. Retrovirology 2012, 9:82.
31. Laguette N., Sobhian B., Casartelli N., Ringeard M., Chable-Bessia C., Ségéral E., Yatim A., Emiliani S., Schwartz O., Benkirane M. SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 2011, 474:654-657.
32. Margolis D.M. Histone deacetylase inhibitors and HIV latency. Curr Opin HIV AIDS 2011, 6:25-29.
33. Mattapallil J.J., Douek D.C., Hill B., Nishimura Y., Martin M., Roederer M. Massive infection and loss of memory CD4+ Tcells in multiple tissues during acute SIV infection. Nature 2005, 434:1093-1097.
34. Orenstein J.M., Fox C., Wahl S.M. Macrophages as a source of HIV during opportunistic infections. Science 1997, 276:1857-1861.
35. + Tcells abrogates post-peak decline of viremia in SIV-infected rhesus macaques. J.Clin. Invest. 2011, 121:4433-4445.
36. Pauls E., Jimenez E., Ruiz A., Permanyer M., Ballana E., Costa H., Nascimiento R., Parkhouse R.M., Peña R., Riveiro-Muñoz E., et al. Restriction of HIV-1 replication in primary macrophages by IL-12 and IL-18 through the upregulation of SAMHD1. J.Immunol. 2013, 190:4736-4741.
37. Picker L.J., Hagen S.I., Lum R., Reed-Inderbitzin E.F., Daly L.M., Sylwester A.W., Walker J.M., Siess D.C., Piatak M., Wang C., et al. Insufficient production and tissue delivery of CD4+ memory Tcells in rapidly progressive simian immunodeficiency virus infection. J.Exp. Med. 2004, 200:1299-1314.
38. Robbins C.S., Hilgendorf I., Weber G.F., Theurl I., Iwamoto Y., Figueiredo J.L., Gorbatov R., Sukhova G.K., Gerhardt L.M., Smyth D., et al. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat. Med. 2013, 19:1166-1172.
39. Siliciano J.D., Siliciano R.F. HIV-1 eradication strategies: design and assessment. Curr Opin HIV AIDS 2013, 8:318-325.
40. Smith P.D., Meng G., Salazar-Gonzalez J.F., Shaw G.M. Macrophage HIV-1 infection and the gastrointestinal tract reservoir. J.Leukoc. Biol. 2003, 74:642-649.
41. Spits H. Development of alphabeta Tcells in the human thymus. Nat. Rev. Immunol. 2002, 2:760-772.
42. Thompson K.A., Cherry C.L., Bell J.E., McLean C.A. Brain cell reservoirs of latent virus in presymptomatic HIV-infected individuals. Am. J. Pathol. 2011, 179:1623-1629.
43. van Furth R. Origin and turnover of monocytes and macrophages. Curr. Top. Pathol. 1989, 79:125-150.
44. Veazey R.S., DeMaria M., Chalifoux L.V., Shvetz D.E., Pauley D.R., Knight H.L., Rosenzweig M., Johnson R.P., Desrosiers R.C., Lackner A.A. Gastrointestinal tract as a major site of CD4+ Tcell depletion and viral replication in SIV infection. Science 1998, 280:427-431.
45. Wang T.H., Donaldson Y.K., Brettle R.P., Bell J.E., Simmonds P. Identification of shared populations of human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system. J.Virol. 2001, 75:11686-11699.
46. Westmoreland S.V., Converse A.P., Hrecka K., Hurley M., Knight H., Piatak M., Lifson J., Mansfield K.G., Skowronski J., Desrosiers R.C. SIV vpx is essential for macrophage infection but not for development of AIDS. PLoS ONE 2014, 9:e84463.
47. Wu F., Ourmanov I., Kuwata T., Goeken R., Brown C.R., Buckler-White A., Iyengar R., Plishka R., Aoki S.T., Hirsch V.M. Sequential evolution and escape from neutralization of simian immunodeficiency virus SIVsmE660 clones in rhesus macaques. J.Virol. 2012, 86:8835-8847.
48. Wynn T.A., Chawla A., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496:445-455.
49. Yao R., Schneider E. Detection of B- and T-cell-specific gene rearrangements in 13 cell lines and 50 clinical specimens using the BIOMED-2 and the original InVivoScribe primers. Leuk. Lymphoma 2007, 48:837-840.