An NK cell population lacking FcRγ is expanded in chronically infected HIV patient

Journal of Immunology

Volumn 194, Issue 10, 2015, Pages 4688-4697

  Zhou, Jingling ^a   Amran, Fathiah S ^b   Kramski, Marit ^c   Angelovich, Tom A ^a,d   Elliott, Julian ^e   Hearps, Anna C ^a,e   Price, Patricia ^b,f   Jaworowski, Anthony ^a,e  

^a BURNET INSTITUTE   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d RMIT UNIVERSITY   (Australia)

^e MONASH UNIVERSITY   (Australia)

^f CURTIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CD16 ANTIGEN; CD56 ANTIGEN; CYTOMEGALOVIRUS ANTIBODY; FC RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; PEPTIDE DERIVATIVE; RITUXIMAB;

ADULT; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY TITER; ANTIGEN EXPRESSION; ARTICLE; CELL EXPANSION; CHRONIC DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CYTOMEGALOVIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; LYMPHOCYTE SUBPOPULATION; MALE; NATURAL KILLER CELL; NONHUMAN; OPSONIZATION; PREVALENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAJI CELL LINE; VIREMIA; ENZYME LINKED IMMUNOSORBENT ASSAY; HIV INFECTIONS; IMMUNOLOGY;

ANTI-RETROVIRAL AGENTS; CHRONIC DISEASE; CROSS-SECTIONAL STUDIES; ENZYME-LINKED IMMUNOSORBENT ASSAY; HIV INFECTIONS; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE SUBSETS; RECEPTORS, IGG;

EID: 84929121168     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402448     Document Type: Article

References (55)

1. Smith, C. J., L. Ryom, R. Weber, P. Morlat, C. Pradier, P. Reiss, J. D. Kowalska, S. de Wit, M. Law, W. el Sadr, et al; D:A:D Study Group. 2014. Trends in underlying causes of death in people with HIV from 1999 to 2011 (D:A:D): a multicohort collaboration. Lancet 384: 241-248.
2. Hearps, A. C., A. Maisa, W. J. Cheng, T. A. Angelovich, G. F. Lichtfuss, C. S. Palmer, A. L. Landay, A. Jaworowski, and S. M. Crowe. 2012. HIV infection induces age-related changes to monocytes and innate immune activation in young men that persist despite combination antiretroviral therapy. AIDS 26: 843-853.
3. Martin, G. E., M. Gouillou, A. C. Hearps, T. A. Angelovich, A. C. Cheng, F. Lynch, W. J. Cheng, G. Paukovics, C. S. Palmer, R. M. Novak, et al. 2013. Age-associated changes in monocyte and innate immune activation markers occur more rapidly in HIV infected women. PLoS ONE 8: e55279.
4. Brenchley, J. M., D. A. Price, T. W. Schacker, T. E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, E. Bornstein, O. Lambotte, D. Altmann, et al. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12: 1365-1371.
5. Dentone, C., A. Di Biagio, A. Parodi, F. Bozzano, P. Fraccaro, A. Signori, G. Cenderello, E. Mantia, G. Orofino, A. De Maria, et al. 2014. Innate immunity cell activation in virologically suppressed HIV-infected maraviroc-treated patients. AIDS 28: 1071-1074.
6. O'Brien, M., E. Montenont, L. Hu, M. A. Nardi, V. Valdes, M. Merolla, G. Gettenberg, K. Cavanagh, J. A. Aberg, N. Bhardwaj, and J. S. Berger. 2013. Aspirin attenuates platelet activation and immune activation in HIV-1-infected subjects on antiretroviral therapy: a pilot study. J. Acquir. Immune Defic. Syndr. 63: 280-288.
7. Burdo, T. H., J. Lo, S. Abbara, J. Wei, M. E. DeLelys, F. Preffer, E. S. Rosenberg, K. C. Williams, and S. Grinspoon. 2011. Soluble CD163, a novel marker of activated macrophages, is elevated and associated with non-calcified coronary plaque in HIV-infected patients. J. Infect. Dis. 204: 1227-1236.
8. Sandler, N. G., H. Wand, A. Roque, M. Law, M. C. Nason, D. E. Nixon, C. Pedersen, K. Ruxrungtham, S. R. Lewin, S. Emery, et al INSIGHT SMART Study Group. 2011. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J. Infect. Dis. 203: 780-790.
9. Krishnan, S., E. M. Wilson, V. Sheikh, A. Rupert, D. Mendoza, J. Yang, R. Lempicki, S. A. Migueles, and I. Sereti. 2014. Evidence for innate immune system activation in HIV type 1-infected elite controllers. J. Infect. Dis. 209: 931-939.
10. Maldarelli, F., S. Palmer, M. S. King, A. Wiegand, M. A. Polis, J. Mican, J. A. Kovacs, R. T. Davey, D. Rock-Kress, R. Dewar, et al. 2007. ART suppresses plasma HIV-1 RNA to a stable set point predicted by pretherapy viremia. PLoS Pathog. 3: e46.
11. Hatano, H., E. L. Delwart, P. J. Norris, T. H. Lee, T. B. Neilands, C. F. Kelley, P. W. Hunt, R. Hoh, J. M. Linnen, J. N. Martin, et al. 2010. Evidence of persistent low-level viremia in long-term HAART-suppressed, HIV-infected individuals. AIDS 24: 2535-2539.
12. + T cell recovery on antiretroviral therapy. J. Infect. Dis. 203: 1474-1483.
13. Wittkop, L., J. Bitard, E. Lazaro, D. Neau, F. Bonnet, P. Mercie, M. Dupon, M. Hessamfar, M. Ventura, D. Malvy, et al; Groupe d'Epidémiologie Clinique du SIDA en Aquitaine. 2013. Effect of cytomegalovirus-induced immune response, self antigen-induced immune response, and microbial translocation on chronic immune activation in successfully treated HIV type 1-infected patients: the ANRS CO3 Aquitaine Cohort. J. Infect. Dis. 207: 622-627.
14. Hazenberg, M. D., and H. Spits. 2014. Human innate lymphoid cells. Blood 124: 700-709.
15. Ferlazzo, G., and C. Münz. 2004. NK cell compartments and their activation by dendritic cells. J. Immunol. 172: 1333-1339.
16. bright NK cells in treatment-naive HIV-1-seropositive individuals. J. Clin. Immunol. 22: 176-183.
17. -/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc. Natl. Acad. Sci. USA 102: 2886-2891.
18. Björkström, N. K., H. G. Ljunggren, and J. K. Sandberg. 2010. CD56 negative NK cells: origin, function, and role in chronic viral disease. Trends Immunol. 31: 401-406.
19. Gonzalez, V. D., K. Falconer, N. K. Björkström, K. G. Blom, O. Weiland, H. G. Ljunggren, A. Alaeus, and J. K. Sandberg. 2009. Expansion of functionally skewed CD56-negative NK cells in chronic hepatitis C virus infection: correlation with outcome of pegylated IFN-α and ribavirin treatment. J. Immunol. 183: 6612-6618.
20. Lanier, L. L. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9: 495-502.
21. Lichtfuss, G. F., A. C. Meehan, W. J. Cheng, P. U. Cameron, S. R. Lewin, S. M. Crowe, and A. Jaworowski. 2011. HIV inhibits early signal transduction events triggered by CD16 cross-linking on NK cells, which are important for antibody-dependent cellular cytotoxicity. J. Leukoc. Biol. 89: 149-158.
22. Alter, G., N. Teigen, B. T. Davis, M. M. Addo, T. J. Suscovich, M. T. Waring, H. Streeck, M. N. Johnston, K. D. Staller, M. T. Zaman, et al. 2005. Sequential deregulation of NK cell subset distribution and function starting in acute HIV-1 infection. Blood 106: 3366-3369.
23. Mavilio, D., J. Benjamin, M. Daucher, G. Lombardo, S. Kottilil, M. A. Planta, E. Marcenaro, C. Bottino, L. Moretta, A. Moretta, and A. S. Fauci. 2003. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc. Natl. Acad. Sci. USA 100: 15011-15016.
24. Mela, C. M., C. T. Burton, N. Imami, M. Nelson, A. Steel, B. G. Gazzard, F. M. Gotch, and M. R. Goodier. 2005. Switch from inhibitory to activating NKG2 receptor expression in HIV-1 infection: lack of reversion with highly active antiretroviral therapy. AIDS 19: 1761-1769.
25. Brunetta, E., M. Fogli, S. Varchetta, L. Bozzo, K. L. Hudspeth, E. Marcenaro, A. Moretta, and D. Mavilio. 2010. Chronic HIV-1 viremia reverses NKG2A/NKG2C ratio on natural killer cells in patients with human cytomegalovirus coinfection. AIDS 24: 27-34.
26. Parato, K. G., A. Kumar, A. D. Badley, J. L. Sanchez-Dardon, K. A. Chambers, C. D. Young, W. T. Lim, S. Kravcik, D. W. Cameron, and J. B. Angel. 2002. Normalization of natural killer cell function and phenotype with effective anti-HIV therapy and the role of IL-10. AIDS 16: 1251-1256.
27. Leeansyah, E., J. Zhou, G. Paukovics, S. R. Lewin, S. M. Crowe, and A. Jaworowski. 2010. Decreased NK cell FcRγ in HIV-1 infected individuals receiving combination antiretroviral therapy: a cross sectional study. PLoS ONE 5: e9643.
28. Lichtfuss, G. F., W. J. Cheng, Y. Farsakoglu, G. Paukovics, R. Rajasuriar, P. Velayudham, M. Kramski, A. C. Hearps, P. U. Cameron, S. R. Lewin, et al. 2012. Virologically suppressed HIV patients show activation of NK cells and persistent innate immune activation. J. Immunol. 189: 1491-1499.
29. Stratov, I., A. Chung, and S. J. Kent. 2008. Robust NK cell-mediated human immunodeficiency virus (HIV)-specific antibody-dependent responses in HIV-infected subjects. J. Virol. 82: 5450-5459.
30. Zhang, T., J. M. Scott, I. Hwang, and S. Kim. 2013. Cutting edge: antibody-dependent memory-like NK cells distinguished by FcRγ deficiency. J. Immunol. 190: 1402-1406.
31. Hibbs, M. L., P. Selvaraj, O. Carpén, T. A.Springer, H. Kuster, M. H. Jouvin, and J. P. Kinet. 1989. Mechanisms for regulating expression of membrane isoforms of FcγRIII (CD16). Science 246: 1608-1611.
32. Fiebiger, E., D. Tortorella, M. H. Jouvin, J. P. Kinet, and H. L. Ploegh. 2005. Cotranslational endoplasmic reticulum assembly of FcεRI controls the formation of functional IgE-binding receptors. J. Exp. Med. 201: 267-277.
33. Lobato-Pascual, A., P. C. Saether, S. Fossum, E. Dissen, and M. R. Daws. 2013. Mincle, the receptor for mycobacterial cord factor, forms a functional receptor complex with MCL and FcaεRI-γ. Eur. J. Immunol. 43: 3167-3174.
34. Kanazawa, N., K. Tashiro, K. Inaba, and Y. Miyachi. 2003. Dendritic cell immunoactivating receptor, a novel C-type lectin immunoreceptor, acts as an activating receptor through association with Fc receptor gamma chain. J. Biol. Chem. 278: 32645-32652.
35. Takai, T. 1996. Multiple loss of effector cell functions in FcRγ-deficient mice. Int. Rev. Immunol. 13: 369-381.
36. dim NK cells. Blood 116: 1299-1307.
37. dim NK-cell differentiation uncoupled from NK-cell education. Blood 116: 3853-3864.
38. Liu, Q., Y. Sun, S. Rihn, A. Nolting, P. N. Tsoukas, S. Jost, K. Cohen, B. Walker, and G. Alter. 2009. Matrix metalloprotease inhibitors restore impaired NK cell-mediated antibody-dependent cellular cytotoxicity in human immunodeficiency virus type 1 infection. J. Virol. 83: 8705-8712.
39. Romee, R., B. Foley, T. Lenvik, Y. Wang, B. Zhang, D. Ankarlo, X. Luo, S. Cooley, M. Verneris, B. Walcheck, and J. Miller. 2013. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood 121: 3599-3608.
40. Metes, D., L. K. Ernst, W. H. Chambers, A. Sulica, R. B. Herberman, and P. A. Morel. 1998. Expression of functional CD32 molecules on human NK cells is determined by an allelic polymorphism of the FcgammaRIIC gene. Blood 91: 2369-2380.
41. Gómez-Román, V. R., L. J. Patterson, D. Venzon, D. Liewehr, K. Aldrich, R. Florese, and M. Robert-Guroff. 2005. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J. Immunol. 174: 2185-2189.
42. Forthal, D. N., and C. Moog. 2009. Fc receptor-mediated antiviral antibodies. Curr Opin HIV AIDS 4: 388-393.
43. Acharya, P., W. D. Tolbert, N. Gohain, X. Wu, L. Yu, T. Liu, W. Huang, C.-C. Huang, Y. D. Kwon, R. K. Louder, et al. 2014. Structural definition of an antibody-dependent cellular cytotoxicity (ADCC) response implicated in reduced risk for HIV-1 infection. J. Virol. 88: 12895-12906.
44. Kuri-Cervantes, L., G. S. de Oca, S. Avila-Ríos, R. Hernández-Juan, and G. Reyes-Terán. 2014. Activation of NK cells is associated with HIV-1 disease progression. J. Leukoc. Biol. 96: 7-16.
45. Malavasi, F., S. Deaglio, A. Funaro, E. Ferrero, A. L. Horenstein, E. Ortolan, T. Vaisitti, and S. Aydin. 2008. Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol. Rev. 88: 841-886.
46. Mallone, R., A. Funaro, M. Zubiaur, G. Baj, C. M. Ausiello, C. Tacchetti, J. Sancho, C. Grossi, and F. Malavasi. 2001. Signaling through CD38 induces NK cell activation. Int. Immunol. 13: 397-409.
47. De Maria, A., M. Fogli, P. Costa, G. Murdaca, F. Puppo, D. Mavilio, A. Moretta, and L. Moretta. 2003. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur. J. Immunol. 33: 2410-2418.
48. Eller, M. A., L. A. Eller, B. J. Ouma, D. Thelian, V. D. Gonzalez, D. Guwatudde, F. E. McCutchan, M. A. Marovich, N. L. Michael, M. S. de Souza, et al. 2009. Elevated natural killer cell activity despite altered functional and phenotypic profile in Ugandans with HIV-1 clade A or clade D infection. J. Acquir. Immune Defic. Syndr. 51: 380-389.
49. Bisio, F., F. Bozzano, F. Marras, A. Di Biagio, L. Moretta, and A. De Maria. 2013. Successfully treated HIV-infected patients have differential expression of NK cell receptors (NKp46 and NKp30) according to AIDS status at presentation. Immunol. Lett. 152: 16-24.
50. Pende, D., S. Parolini, A. Pessino, S. Sivori, R. Augugliaro, L. Morelli, E. Marcenaro, L. Accame, A. Malaspina, R. Biassoni, et al. 1999. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J. Exp. Med. 190: 1505-1516.
51. Arnon, T. I., H. Achdout, O. Levi, G. Markel, N. Saleh, G. Katz, R. Gazit, T. Gonen-Gross, J. Hanna, E. Nahari, et al. 2005. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat. Immunol. 6: 515-523.
52. Vitale, M., C. Bottino, S. Sivori, L. Sanseverino, R. Castriconi, E. Marcenaro, R. Augugliaro, L. Moretta, and A. Moretta. 1998. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J. Exp. Med. 187: 2065-2072.
53. Pessino, A., S. Sivori, C. Bottino, A. Malaspina, L. Morelli, L. Moretta, R. Biassoni, and A. Moretta. 1998. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J. Exp. Med. 188: 953-960.
54. Li, S. S., S. K. Kyei, M. Timm-McCann, H. Ogbomo, G. J. Jones, M. Shi, R. F. Xiang, P. Oykhman, S. M. Huston, A. Islam, et al. 2013. The NK receptor NKp30 mediates direct fungal recognition and killing and is diminished in NK cells from HIV-infected patients. Cell Host Microbe 14: 387-397.
55. De Maria, A., and L. Moretta. 2008. NK cell function in HIV-1 infection. Curr. HIV Res. 6: 433-440.