The immunosuppressive domain of the transmembrane envelope protein gp41 of HIV-1 binds to human monocytes and B cells

Immunologic Research

Volumn 64, Issue 3, 2016, Pages 721-729

  Mühle, Michael ^a   Kroniger, Tobias ^a   Hoffmann, Kerstin ^b   Denner, Joachim ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

^b Berlin Brandenburg Center for Regenerative Therapies   (Germany)

Author keywords

gp41; HIV 1; Immunosuppression; PBMC subsets; TM

Indexed keywords

GLYCOPROTEIN GP 41; MEMBRANE PROTEIN; POLYMER; IMMUNOGLOBULIN RECEPTOR; IMMUNOSUPPRESSIVE AGENT; PEPTIDE; PROTEIN BINDING;

ARTICLE; B LYMPHOCYTE; BINDING SITE; CELL VIABILITY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; CELL LINE; CELL MEMBRANE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; POLYMERIZATION;

B-LYMPHOCYTES; CELL LINE; CELL MEMBRANE; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOMODULATION; IMMUNOSUPPRESSIVE AGENTS; MONOCYTES; PEPTIDES; POLYMERIZATION; PROTEIN BINDING; PROTEIN DOMAINS; RECEPTORS, IMMUNOLOGIC;

EID: 84954111076     PISSN: 0257277X     EISSN: 15590755     Source Type: Journal    
DOI: 10.1007/s12026-015-8776-4     Document Type: Article

References (38)

1. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med. 2004;200(6):749–59. doi:10.1084/jem.20040874.
2. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12(12):1365–71. doi:10.1038/nm1511.
3. Dinh DM, Volpe GE, Duffalo C, Bhalchandra S, Tai AK, Kane AV, et al. Intestinal microbiota, microbial translocation, and systemic inflammation in chronic HIV infection. J Infect Dis. 2015;211(1):19–27. doi:10.1093/infdis/jiu409.
4. Klatt NR, Funderburg NT, Brenchley JM. Microbial translocation, immune activation, and HIV disease. Trends Microbiol. 2013;21(1):6–13. doi:10.1016/j.tim.2012.09.001.
5. Dyavar Shetty R, Velu V, Titanji K, Bosinger SE, Freeman GJ, Silvestri G, et al. PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques. J Clin Invest. 2012;122(5):1712–6. doi:10.1172/JCI60612.
6. Estes JD. Enhancing immune responses to limit chronic immune activation during SIV. J Clin Invest. 2012;122(5):1611–4. doi:10.1172/JCI63389.
7. Maartens G, Celum C, Lewin SR. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet. 2014;384(9939):258–71. doi:10.1016/S0140-6736(14)60164-1.
8. Denner J. The transmembrane proteins contribute to immunodeficiencies induced by HIV-1 and other retroviruses. AIDS. 2014;28(8):1081–90. doi:10.1097/QAD.0000000000000195.
9. Blaise S, Mangeney M, Heidmann T. The envelope of Mason-Pfizer monkey virus has immunosuppressive properties. J Gen Virol. 2001;82(Pt 7):1597–600. doi:10.1099/0022-1317-82-7-1597.
10. Mangeney M, de Parseval N, Thomas G, Heidmann T. The full-length envelope of an HERV-H human endogenous retrovirus has immunosuppressive properties. J Gen Virol. 2001;82(Pt 10):2515–8. doi:10.1099/0022-1317-82-10-2515.
11. Mangeney M, Heidmann T. Tumor cells expressing a retroviral envelope escape immune rejection in vivo. Proc Natl Acad Sci U S A. 1998;95(25):14920–5.
12. Schlecht-Louf G, Renard M, Mangeney M, Letzelter C, Richaud A, Ducos B, et al. Retroviral infection in vivo requires an immune escape virulence factor encrypted in the envelope protein of oncoretroviruses. Proc Natl Acad Sci U S A. 2010;107(8):3782–7. doi:10.1073/pnas.0913122107.
13. Mangeney M, Pothlichet J, Renard M, Ducos B, Heidmann T. Endogenous retrovirus expression is required for murine melanoma tumor growth in vivo. Cancer Res. 2005;65(7):2588–91. doi:10.1158/0008-5472.CAN-04-4231.
14. Denner J, Eschricht M, Lauck M, Semaan M, Schlaermann P, Ryu H, et al. Modulation of cytokine release and gene expression by the immunosuppressive domain of gp41 of HIV-1. PLoS One. 2013;8(1):e55199. doi:10.1371/journal.pone.0055199.
15. Morozov VA, Morozov AV, Semaan M, Denner J. Single mutations in the transmembrane envelope protein abrogate the immunosuppressive property of HIV-1. Retrovirology. 2012;9:67. doi:10.1186/1742-4690-9-67.
16. Chen YH, Bock G, Vornhagen R, Steindl F, Katinger H, Dierich MP. HIV-1 gp41 binds to several proteins on the human B-cell line Raji. Mol Immunol. 1993;30(13):1159–63.
17. Chen YH, Bock G, Vornhagen R, Steindl F, Katinger H, Dierich MP. The human monocyte cell line U937 binds HIV-1 gp41 by proteins of 37, 45, 49, 62 and 92 kDa. Immunol Lett. 1993;37(1):41–5.
18. Chen YH, Ebenbichler C, Vornhagen R, Schulz TF, Steindl F, Bock G, et al. HIV-1 gp41 contains two sites for interaction with several proteins on the helper T-lymphoid cell line, H9. AIDS. 1992;6(6):533–9.
19. Henderson LA, Qureshi MN. A peptide inhibitor of human immunodeficiency virus infection binds to novel human cell surface polypeptides. J Biol Chem. 1993;268(20):15291–7.
20. Chen YH, Wu W, Yang J, Sui SF, Sun J, Dierich MP. Antibodies against human IFN-alpha and -beta recognized the immunosuppressive domain of HIV-1 gp41 and inhibit gp41-binding to the putative cellular receptor protein p45. Immunol Lett. 1999;69(2):253–7.
21. Yu T, Xiao Y, Bai Y, Ru Q, Luo G, Dierich MP, et al. Human interferon-beta inhibits binding of HIV-1 gp41 to lymphocyte and monocyte cells and binds the potential receptor protein P50 for HIV-1 gp41. Immunol Lett. 2000;73(1):19–22.
22. Speth C, Prohaszka Z, Mair M, Stockl G, Zhu X, Jobstl B, et al. A 60 kD heat-shock protein-like molecule interacts with the HIV transmembrane glycoprotein gp41. Mol Immunol. 1999;36(9):619–28.
23. Ebenbichler CF, Thielens NM, Vornhagen R, Marschang P, Arlaud GJ, Dierich MP. Human immunodeficiency virus type 1 activates the classical pathway of complement by direct C1 binding through specific sites in the transmembrane glycoprotein gp41. J Exp Med. 1991;174(6):1417–24.
24. Thielens NM, Bally IM, Ebenbichler CF, Dierich MP, Arlaud GJ. Further characterization of the interaction between the C1q subcomponent of human C1 and the transmembrane envelope glycoprotein gp41 of HIV-1. J Immunol. 1993;151(11):6583–92.
25. Qureshi NM, Coy DH, Garry RF, Henderson LA. Characterization of a putative cellular receptor for HIV-1 transmembrane glycoprotein using synthetic peptides. AIDS. 1990;4(6):553–8.
26. Denner J, Vogel T, Norley S, Ennen J, Kurth R. The immunosuppressive (ISU-) peptide of HIV-1: binding to lymphocyte surface proteins. J Cancer Res Clin Oncol. 1993;119(S1):28.
27. Denner J, Vogel T, Norley S, Kurth R. The immunosuppressive peptide of HIV-1 inhibits T and B lymphocyte proliferation, inhibits HIV-1 replication and binds to lymphocyte receptor proteins. AIDS Res Hum Retroviruses 1995;11(S1):195.
28. Cianciolo GJ, Copeland TD, Oroszlan S, Snyderman R. Inhibition of lymphocyte proliferation by a synthetic peptide homologous to retroviral envelope proteins. Science. 1985;230(4724):453–5.
29. Denner J, Persin C, Vogel T, Haustein D, Norley S, Kurth R. The immunosuppressive peptide of HIV-1 inhibits T and B lymphocyte stimulation. J Acquir Immune Defic Syndr Hum Retrovirol. 1996;12(5):442–50.
30. Ruegg CL, Monell CR, Strand M. Inhibition of lymphoproliferation by a synthetic peptide with sequence identity to gp41 of human immunodeficiency virus type 1. J Virol. 1989;63(8):3257–60.
31. Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN, et al. Nomenclature of monocytes and dendritic cells in blood. Blood. 2010;116(16):e74–80. doi:10.1182/blood-2010-02-258558.
32. Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K. Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer. 1980;26(2):171–6.
33. Salahuddin SZ, Markham PD, Wong-Staal F, Franchini G, Kalyanaraman VS, Gallo RC. Restricted expression of human T-cell leukemia–lymphoma virus (HTLV) in transformed human umbilical cord blood lymphocytes. Virology. 1983;129(1):51–64.
34. Barcova M, Kacani L, Speth C, Dierich MP. gp41 envelope protein of human immunodeficiency virus induces interleukin (IL)-10 in monocytes, but not in B, T, or NK cells, leading to reduced IL-2 and interferon-gamma production. J Infect Dis. 1998;177(4):905–13.
35. Denner J, Norley S, Kurth R. The immunosuppressive peptide of HIV-1: functional domains and immune response in AIDS patients. AIDS. 1994;8(8):1063–72.
36. Ellery PJ, Tippett E, Chiu YL, Paukovics G, Cameron PU, Solomon A, et al. The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J Immunol. 2007;178(10):6581–9.
37. Fischer-Smith T, Croul S, Sverstiuk AE, Capini C, L’Heureux D, Regulier EG, et al. CNS invasion by CD14 +/CD16+ peripheral blood-derived monocytes in HIV dementia: perivascular accumulation and reservoir of HIV infection. J Neurovirol. 2001;7(6):528–41. doi:10.1080/135502801753248114.
38. Pulliam L, Gascon R, Stubblebine M, McGuire D, McGrath MS. Unique monocyte subset in patients with AIDS dementia. Lancet. 1997;349(9053):692–5. doi:10.1016/S0140-6736(96)10178-1.