CD32-expressing CD4 T cells are phenotypically diverse and can contain proviral HIV DNA

Frontiers in Immunology

Volumn 9, Issue MAY, 2018, Pages

  Martin, Genevieve E ^a   Pace, Matthew ^a   Thornhill, John P ^a,b   Phetsouphanh, Chansavath ^a   Meyerowitz, Jodi ^a   Gossez, Morgane ^a   Brown, Helen ^a   Olejniczak, Natalia ^a   Lwanga, Julianne ^c   Ramjee, Gita ^d   Kaleebu, Pontiano ^e   Porter, Kholoud ^f   Willberg, Christian B ^a,g   Klenerman, Paul ^a,g   Nwokolo, Nneka ^h   Fox, Julie ^c,j   Fidler, Sarah ^b   Frater, John ^a,g   Lever, Andrew ⁱ   Wills, Mark ⁱ   Weber, Jonathan ^b   Dorrell, Lucy ^g   Malim, Mike ^j   Gupta, Ravi ^f   Jolly, Clare ^f   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^d SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

^e UGANDA VIRUS RESEARCH INSTITUTE   (Uganda)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

ⁱ UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^j KING'S COLLEGE LONDON   (United Kingdom)

more..

Author keywords

CD32; HIV; HIV DNA; Primary HIV infection; Reservoir

Indexed keywords

BIOLOGICAL MARKER; CD20 ANTIGEN; CD3 ANTIBODY; CD32 ANTIGEN; CD4 ANTIBODY; HLA DR ANTIGEN; IMMUNOGLOBULIN; T LYMPHOCYTE RECEPTOR; VIRUS DNA;

ACUTE HIV INFECTION; ADULT; ANTIRETROVIRAL THERAPY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC MARKER; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; MALE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROLOGY; VIREMIA; VIRUS LOAD;

EID: 85046619344     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.00928     Document Type: Article

References (44)

1. Wherry EJ, Kurachi M. Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol (2015) 15(8):486-99. doi:10.1038/nri3862
2. Trautmann L, Janbazian L, Chomont N, Said EA, Gimmig S, Bessette B, et al. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med (2006) 12(10):1198-202. doi:10.1038/nm1106-1329b
3. Jones RB, Ndhlovu LC, Barbour JD, Sheth PM, Jha AR, Long BR, et al. Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med (2008) 205(12):2763-79. doi:10.1084/jem.20081398
4. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, Reddy S, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature (2006) 443(7109):350-4. doi:10.1038/nature05115
5. Chew GM, Fujita T, Webb GM, Burwitz BJ, Wu HL, Reed JS, et al. TIGIT marks exhausted T cells, correlates with disease progression, and serves as a target for immune restoration in HIV and SIV infection. PLoS Pathog (2016) 12(1):e1005349. doi:10.1371/journal.ppat.1005349
6. Hurst J, Hoffmann M, Pace M, Williams JP, Thornhill J, Hamlyn E, et al. Immunological biomarkers predict HIV-1 viral rebound after treatment interruption. Nat Commun (2015) 6:8495. doi:10.1038/ncomms9495
7. Hoffmann M, Pantazis N, Martin GE, Hickling S, Hurst J, Meyerowitz J, et al. Exhaustion of activated CD8 T cells predicts disease progression in primary HIV-1 infection. PLoS Pathog (2016) 12(7):e1005661. doi:10.1371/journal.ppat.1005661
8. Fromentin R, Bakeman W, Lawani MB, Khoury G, Hartogensis W, DaFonseca S, et al. CD4+ T cells expressing PD-1, TIGIT and LAG-3 contribute to HIV persistence during ART. PLoS Pathog (2016) 12(7):e1005761. doi:10.1371/journal.ppat.1005761
9. Chomont N, El-Far M, Ancuta P, Trautmann L, Procopio FA, Yassine-Diab B, et al. HIV reservoir size and persistence are driven by T cell survival and homeostatic proliferation. Nat Med (2009) 15(8):893-900. doi:10.1038/nm.1972
10. Hogarth PM, Pietersz GA. Fc receptor-targeted therapies for the treatment of inflammation, cancer and beyond. Nat Rev Drug Discov (2012) 11(4):311-31. doi:10.1038/nrd2909
11. Descours B, Petitjean G, Lopez-Zaragoza JL, Bruel T, Raffel R, Psomas C, et al. CD32a is a marker of a CD4 T-cell HIV reservoir harbouring replication-competent proviruses. Nature (2017) 543(7646):564-7. doi:10.1038/nature21710
12. Sandor M, Lynch RG. Lymphocyte Fc receptors: the special case of T cells. Immunol Today (1993) 14(5):227-31. doi:10.1016/0167-5699(93)90168-K
13. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol (2008) 8(1):34-47. doi:10.1038/nri2206
14. Chauhan AK. Human CD4(+) T-cells: a role for low-affinity Fc receptors. Front Immunol (2016) 7:215. doi:10.3389/fimmu.2016.00215
15. Sandilands GP, MacPherson SA, Burnett ER, Russell AJ, Downie I, MacSween RN. Differential expression of CD32 isoforms following alloactivation of human T cells. Immunology (1997) 91(2):204-11. doi:10.1046/j.1365-2567.1997.00241.x
16. Engelhardt W, Matzke J, Schmidt RE. Activation-dependent expression of low affinity IgG receptors Fc gamma RII(CD32) and Fc gamma RIII(CD16) in subpopulations of human T lymphocytes. Immunobiology (1995) 192(5):297-320. doi:10.1016/S0171-2985(11)80172-5
17. Starbeck-Miller GR, Badovinac VP, Barber DL, Harty JT. Cutting edge: expression of FcgammaRIIB tempers memory CD8 T cell function in vivo. J Immunol (2014) 192(1):35-9. doi:10.4049/jimmunol.1302232
18. Jain V, Hartogensis W, Bacchetti P, Hunt PW, Hatano H, Sinclair E, et al. Antiretroviral therapy initiated within 6 months of HIV infection is associated with lower T-cell activation and smaller HIV reservoir size. J Infect Dis (2013) 208(8):1202-11. doi:10.1093/infdis/jit311
19. Buzon MJ, Martin-Gayo E, Pereyra F, Ouyang Z, Sun H, Li JZ, et al. Long-term antiretroviral treatment initiated at primary HIV-1 infection affects the size, composition, and decay kinetics of the reservoir of HIV-1-infected CD4 T cells. J Virol (2014) 88(17):10056-65. doi:10.1128/JVI.01046-14
20. Ananworanich J, Schuetz A, Vandergeeten C, Sereti I, de Souza M, Rerknimitr R, et al. Impact of multi-targeted antiretroviral treatment on gut T cell depletion and HIV reservoir seeding during acute HIV infection. PLoS One (2012) 7(3):e33948. doi:10.1371/journal.pone.0033948
21. SPARTAC Trial Investigators, Fidler S, Porter K, Ewings F, Frater J, Ramjee G, et al. Short-course antiretroviral therapy in primary HIV infection. N Engl J Med (2013) 368(3):207-17. doi:10.1056/NEJMoa1110039
22. Williams JP, Hurst J, Stohr W, Robinson N, Brown H, Fisher M, et al. HIV-1 DNA predicts disease progression and post-treatment virological control. Elife (2014) 3:e03821. doi:10.7554/eLife.03821
23. Jones M, Williams J, Gartner K, Phillips R, Hurst J, Frater J. Low copy target detection by Droplet Digital PCR through application of a novel open access bioinformatic pipeline, 'definetherain'. J Virol Methods (2014) 202:46-53. doi:10.1016/j.jviromet.2014.02.020
24. Zamora C, Canto E, Nieto JC, Ortiz MA, Diaz-Torne C, Diaz-Lopez C, et al. Functional consequences of platelet binding to T lymphocytes in inflammation. J Leukoc Biol (2013) 94(3):521-9. doi:10.1189/jlb.0213074
25. Tangye SG, Avery DT, Deenick EK, Hodgkin PD. Intrinsic differences in the proliferation of naive and memory human B cells as a mechanism for enhanced secondary immune responses. J Immunol (2003) 170(2):686. doi:10.4049/jimmunol.170.2.686
26. Wilk E, Witte T, Marquardt N, Horvath T, Kalippke K, Scholz K, et al. Depletion of functionally active CD20+ T cells by rituximab treatment. Arthritis Rheum (2009) 60(12):3563-71. doi:10.1002/art.24998
27. Schuh E, Berer K, Mulazzani M, Feil K, Meinl I, Lahm H, et al. Features of human CD3+CD20+ T cells. J Immunol (2016) 197(4):1111-7. doi:10.4049/jimmunol.1600089
28. Palanichamy A, Jahn S, Nickles D, Derstine M, Abounasr A, Hauser SL, et al. Rituximab efficiently depletes increased CD20-expressing T cells in multiple sclerosis patients. J Immunol (2014) 193(2):580-6. doi:10.4049/jimmunol.1400118
29. Niu J, Zhai Z, Hao F, Zhang Y, Song Z, Zhong H. Dissection of a circulating CD3(+) CD20(+) T-cell subpopulation in patients with psoriasis. Clin Exp Immunol (2018) 192(2):206-12. doi:10.1111/cei.13106
30. Katopodis O, Liossis SN, Viglis V, Pouli A, Dimopoulos MA, Sfikakis PP. Expansion of CD8+ T cells that express low levels of the B cell-specific molecule CD20 in patients with multiple myeloma. Br J Haematol (2003) 120(3):478-81. doi:10.1046/j.1365-2141.2003.04087.x
31. Eggleton P, Bremer E, Tarr JM, de Bruyn M, Helfrich W, Kendall A, et al. Frequency of Th17 CD20+ cells in the peripheral blood of rheumatoid arthritis patients is higher compared to healthy subjects. Arthritis Res Ther (2011) 13(6):R208. doi:10.1186/ar3541
32. Jaafoura S, de Goer de Herve MG, Hernandez-Vargas EA, Hendel-Chavez H, Abdoh M, Mateo MC, et al. Progressive contraction of the latent HIV reservoir around a core of less-differentiated CD4(+) memory T cells. Nat Commun (2014) 5:5407. doi:10.1038/ncomms6407
33. Siliciano JD, Kajdas J, Finzi D, Quinn TC, Chadwick K, Margolick JB, et al. Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4+ T cells. Nat Med (2003) 9(6):727-8. doi:10.1038/nm880
34. Finzi D, Blankson J, Siliciano JD, Margolick JB, Chadwick K, Pierson T, et al. Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med (1999) 5(5):512-7. doi:10.1038/8394
35. Chun TW, Carruth L, Finzi D, Shen X, DiGiuseppe JA, Taylor H, et al. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature (1997) 387(6629):183-8. doi:10.1038/387183a0
36. Wittner M, Dunay GA, Kummer S, Bockhorn M, Hufner A, Schmiedel S, et al. CD32 expression of different memory T cell subpopulations in the blood and lymph nodal tissue of HIV patients and healthy controls correlates with immune activation. J Acquir Immune Defic Syndr (2018) 77(4):345-9. doi:10.1097/QAI.0000000000001622
37. Grau-Exposito J, Serra-Peinado C, Miguel L, Navarro J, Curran A, Burgos J, et al. A novel single-cell FISH-flow assay identifies effector memory CD4(+) T cells as a major niche for HIV-1 transcription in HIV-infected patients. mBio (2017) 8(4):e00876-17. doi:10.1128/mBio.00876-17
38. Eisele E, Siliciano RF. Redefining the viral reservoirs that prevent HIV-1 eradication. Immunity (2012) 37(3):377-88. doi:10.1016/j.immuni.2012.08.010
39. Chun TW, Finzi D, Margolick J, Chadwick K, Schwartz D, Siliciano RF. In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nat Med (1995) 1(12):1284-90. doi:10.1038/nm1295-1284
40. Shan L, Deng K, Gao H, Xing S, Capoferri AA, Durand CM, et al. Transcriptional reprogramming during effector-to-memory transition renders CD4(+) T cells permissive for latent HIV-1 infection. Immunity (2017) 47(4):766.e-75.e. doi:10.1016/j.immuni.2017.09.014
41. Martin G, Pace M, Thornhill J, Phetsouphanh C, Meyerowitz J, Gossez M, et al. Enrichment of the HIV reservoir in CD32+ CD4 T cells occurs early in blood and tissue. bioRxiv (2017) 169342. doi:10.1101/169342
42. Zandieh A, Izad M, Fakhri M, Amirifard H, Khazaeipour Z, Harirchian MH. Cytometric profiling in various clinical forms of multiple sclerosis with respect to CD21+, CD32+, and CD35+ B and T cells. Transl Neurodegener (2013) 2(1):14. doi:10.1186/2047-9158-2-14
43. Hocqueloux L, Avettand-Fenoel V, Jacquot S, Prazuck T, Legac E, Melard A, et al. Long-term antiretroviral therapy initiated during primary HIV-1 infection is key to achieving both low HIV reservoirs and normal T cell counts. J Antimicrob Chemother (2013) 68(5):1169-78. doi:10.1093/jac/dks533
44. Hey-Cunningham WJ, Murray JM, Natarajan V, Amin J, Moore CL, Emery S, et al. Early antiretroviral therapy with raltegravir generates sustained reductions in HIV reservoirs but not lower T-cell activation levels. AIDS (2015) 29(8):911-9. doi:10.1097/QAD.0000000000000625