NK cell and Ig interplay in defense against herpes simplex virus type 1: Epistatic interaction of CD16A and IgG1 allotypes of variable affinities modulates antibody-dependent cellular cytotoxicity and susceptibility to clinical reactivation

Journal of Immunology

Volumn 195, Issue 4, 2015, Pages 1676-1684

  Moraru, Manuela ^a   Black, Laurel E ^b   Muntasell, Aura ^c   Portero, Francisca ^a   López Botet, Miguel ^c   Reyburn, Hugh T ^d   Pandey, Janardan P ^b   Vilches, Carlos ^a  

^a HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c HOSPITAL DEL MAR   (Spain)

^d CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD16A ANTIGEN; CD32 ANTIGEN; CD32C ANTIGEN; FC RECEPTOR IIB; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G1 H CHAIN; IMMUNOGLOBULIN G1 KAPPA CHAIN; UNCLASSIFIED DRUG; FC GAMMA RECEPTOR IIC; FC RECEPTOR; FCGR3A PROTEIN, HUMAN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN KAPPA CHAIN;

ALLOTYPE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BINDING AFFINITY; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE COURSE; EPISTASIS; FCGR GENE; FIBROBLAST; GENE; GENE CLUSTER; GENE INTERACTION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NATURAL KILLER CELL; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; RISK FACTOR; VIRUS REACTIVATION; ANIMAL; CELL LINE; DEGRANULATION; DISEASE PREDISPOSITION; GENE EXPRESSION; GENETICS; HERPES SIMPLEX; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; VIRUS ACTIVATION;

ANIMALS; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CELL DEGRANULATION; CELL LINE; DISEASE SUSCEPTIBILITY; EPISTASIS, GENETIC; GENE EXPRESSION; GENETIC VARIATION; GENOTYPE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN KAPPA-CHAINS; IMMUNOPHENOTYPING; KILLER CELLS, NATURAL; PHENOTYPE; POLYMORPHISM, GENETIC; RECEPTORS, IGG; VIRUS ACTIVATION;

EID: 84938944485     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500872     Document Type: Article

References (65)

1. Hobbs, M. R., B. B. Jones, B. E. Otterud, M. Leppert, and J. D. Kriesel. 2008. Identification of a herpes simplex labialis susceptibility region on human chromosome 21. J. Infect. Dis. 197: 340-346.
2. Moraru, M., E. Cisneros, N. Gómez-Lozano, R. de Pablo, F. Portero, M. Cañizares, M. Vaquero, G. Roustán, I. Millán, M. López-Botet, and C. Vilches. 2012. Host genetic factors in susceptibility to herpes simplex type 1 virus infection: contribution of polymorphic genes at the interface of innate and adaptive immunity. J. Immunol. 188: 4412-4420.
3. Zhang, S. Y., L. Abel, and J. L. Casanova. 2013. Mendelian predisposition to herpes simplex encephalitis. Handb. Clin. Neurol. 112: 1091-1097.
4. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
5. Mathiesen, T., M. A. Persson, V. A. Sundqvist, and B. Wahren. 1988. Neutralization capacity and antibody dependent cell-mediated cytotoxicity of separated IgG subclasses 1, 3 and 4 against herpes simplex virus. Clin. Exp. Immunol. 72: 211-215.
6. Moraru, M., and C. Vilches. 2015. Host genetics and response to herpes simplex type I infection. In Genomics, Personalized Medicine and Oral Disease. S. T. Sonis, ed. Springer, New York. In press.
7. Atherton, A., K. L. Armour, S. Bell, A. C. Minson, and M. R. Clark. 2000. The herpes simplex virus type 1 Fc receptor discriminates between IgG1 allotypes. Eur. J. Immunol. 30: 2540-2547.
8. Dubin, G., E. Socolof, I. Frank, and H. M. Friedman. 1991. Herpes simplex virus type 1 Fc receptor protects infected cells from antibody-dependent cellular cytotoxicity. J. Virol. 65: 7046-7050.
9. Frank, I., and H. M. Friedman. 1989. A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J. Virol. 63: 4479-4488.
10. Johansson, P. J., T. Hallberg, V. A. Oxelius, A. Grubb, and J. Blomberg. 1984. Human immunoglobulin class and subclass specificity of Fc receptors induced by herpes simplex virus type 1. J. Virol. 50: 796-804.
11. Johnson, D. C., M. C. Frame, M. W. Ligas, A. M. Cross, and N. D. Stow. 1988. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J. Virol. 62: 1347-1354.
12. Nimmerjahn, F., and J. V. Ravetch. 2008. Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8: 34-47.
13. Breunis, W. B., E. van Mirre, J. Geissler, N. Laddach, G. Wolbink, E. van der Schoot, M. de Haas, M. de Boer, D. Roos, and T. W. Kuijpers. 2009. Copy number variation at the FCGR locus includes FCGR3A, FCGR2C and FCGR3B but not FCGR2A and FCGR2B. Hum. Mutat. 30: E640-E650.
14. van Sorge, N. M., W. L. van der Pol, and J. G. van de Winkel. 2003. FcgammaR polymorphisms: implications for function, disease susceptibility and immunotherapy. Tissue Antigens 61: 189-202.
15. van der Heijden, J., W. B. Breunis, J. Geissler, M. de Boer, T. K. van den Berg, and T. W. Kuijpers. 2012. Phenotypic variation in IgG receptors by nonclassical FCGR2C alleles. J. Immunol. 188: 1318-1324.
16. 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.
17. Mueller, M., P. Barros, A. S. Witherden, A. L. Roberts, Z. Zhang, H. Schaschl, C. Y. Yu, M. E. Hurles, C. Schaffner, R. A. Floto, et al. 2013. Genomic pathology of SLE-associated copy-number variation at the FCGR2C/FCGR3B/FCGR2B locus. Am. J. Hum. Genet. 92: 28-40.
18. Wu, J., J. C. Edberg, P. B. Redecha, V. Bansal, P. M. Guyre, K. Coleman, J. E. Salmon, and R. P. Kimberly. 1997. A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J. Clin. Invest. 100: 1059-1070.
19. Sondermann, P., R. Huber, V. Oosthuizen, and U. Jacob. 2000. The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex. Nature 406: 267-273.
20. Radaev, S., S. Motyka, W. H. Fridman, C. Sautes-Fridman, and P. D. Sun. 2001. The structure of a human type III Fcgamma receptor in complex with Fc. J. Biol. Chem. 276: 16469-16477.
21. Breunis, W. B., E. van Mirre, M. Bruin, J. Geissler, M. de Boer, M. Peters, D. Roos, M. de Haas, H. R. Koene, and T. W. Kuijpers. 2008. Copy number variation of the activating FCGR2C gene predisposes to idiopathic thrombocytopenic purpura. Blood 111: 1029-1038.
22. Aitman, T. J., R. Dong, T. J. Vyse, P. J. Norsworthy, M. D. Johnson, J. Smith, J. Mangion, C. Roberton-Lowe, A. J. Marshall, E. Petretto, et al. 2006. Copy number polymorphism in Fcgr3 predisposes to glomerulonephritis in rats and humans. Nature 439: 851-855.
23. Fanciulli, M., P. J. Norsworthy, E. Petretto, R. Dong, L. Harper, L. Kamesh, J. M. Heward, S. C. Gough, A. de Smith, A. I. Blakemore, et al. 2007. FCGR3B copy number variation is associated with susceptibility to systemic, but not organ-specific, autoimmunity. Nat. Genet. 39: 721-723.
24. Pandey, J. P., and Z. Li. 2013. The forgotten tale of immunoglobulin allotypes in cancer risk and treatment. Exp. Hematol. Oncol. 2: 6.
25. Oxelius, V. A., and J. P. Pandey. 2013. Human immunoglobulin constant heavy G chain (IGHG) (Fcg) (GM) genes, defining innate variants of IgG molecules and B cells, have impact on disease and therapy. Clin. Immunol. 149: 475-486.
26. Pandey, J. P. 2000. Immunoglobulin GM and KM allotypes and vaccine immunity. Vaccine 19: 613-617.
27. Lefranc, M. P., and G. Lefranc. 2012. Human Gm, Km, and Am allotypes and their molecular characterization: a remarkable demonstration of polymorphism. Methods Mol. Biol. 882: 635-680.
28. Pandey, J. P. 2012. Immunoglobulin genes and immunity to herpes simplex virus type 1. J. Infect. Dis. 206: 143-144.
29. Armour, K. L., C. S. Smith, and M. R. Clark. 2010. Expression of human FcgammaRIIIa as a GPI-linked molecule on CHO cells to enable measurement of human IgG binding. J. Immunol. Methods 354: 20-33.
30. Moxley, G., and R. S. Gibbs. 1992. Polymerase chain reaction-based genotyping for allotypic markers of immunoglobulin kappa shows allelic association of Km with kappa variable segment. Genomics 13: 104-108.
31. Vilches, C., J. Castaño, P. Muñoz, and J. Peñalver. 2008. Simple genotyping of functional polymorphisms of the human immunoglobulin G receptors CD16A and CD32A: a reference cell panel. Tissue Antigens 71: 242-246.
32. Chisholm, S. E., K. Howard, M. V. Gómez, and H. T. Reyburn. 2007. Expression of ICP0 is sufficient to trigger natural killer cell recognition of herpes simplex virus-infected cells by natural cytotoxicity receptors. J. Infect. Dis. 195: 1160-1168.
33. Balan, P., N. Davis-Poynter, S. Bell, H. Atkinson, H. Browne, and T. Minson. 1994. An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. J. Gen. Virol. 75: 1245-1258.
34. Showalter, S. D., M. Zweig, and B. Hampar. 1981. Monoclonal antibodies to herpes simplex virus type 1 proteins, including the immediate-early protein ICP 4. Infect. Immun. 34: 684-692.
35. Schanfield, M. S., P. Herzog, and H. H. Fudenberg. 1975. Immunoglobulin allotypes of European populations. II. Gm, Am and Km(Inv) allotypic markers in Czechoslovakians. Hum. Hered. 25: 382-392.
36. Schanfield, M. S., J. Gergely, and H. H. Fudenberg. 1975. Immunoglobulin Allotypes of European Populations. I. Gm and Km(Inv) allotypic markers in Hungarians. Hum. Hered. 25: 370-377.
37. Lejeune, J., B. Piègu, V. Gouilleux-Gruart, M. Ohresser, H. Watier, and G. Thibault. 2012. FCGR2C genotyping by pyrosequencing reveals linkage disequilibrium with FCGR3A V158F and FCGR2A H131R polymorphisms in a Caucasian population. MAbs 4: 784-787.
38. Béziat, V., B. Descours, C. Parizot, P. Debré, and V. Vieillard. 2010. NK cell terminal differentiation: correlated stepwise decrease of NKG2A and acquisition of KIRs. PLoS One 5: e11966.
39. Björkström, N. K., P. Riese, F. Heuts, S. Andersson, C. Fauriat, M. A. Ivarsson, A. T. Björklund, M. Flodström-Tullberg, J. Michaëlsson, M. E. Rottenberg, et al. 2010. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 116: 3853-3864.
40. Gumá, M., A. Angulo, C. Vilches, N. Gómez-Lozano, N. Malats, and M. López-Botet. 2004. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104: 3664-3671.
41. López-Botet, M., A. Muntasell, and C. Vilches. 2014. The CD94/NKG2C+ NKcell subset on the edge of innate and adaptive immunity to human cytomegalovirus infection. Semin. Immunol. 26: 145-151.
42. Muntasell, A., M. López-Montañés, A. Vera, G. Heredia, N. Romo, J. Peñafiel, M. Moraru, J. Vila, C. Vilches, and M. López-Botet. 2013. NKG2C zygosity influences CD94/NKG2C receptor function and the NK-cell compartment redistribution in response to human cytomegalovirus. Eur. J. Immunol. 43: 3268-3278.
43. Zhang, T., J. M. Scott, I. Hwang, and S. Kim. 2013. Cutting edge: antibodydependent memory-like NK cells distinguished by FcRg deficiency. J. Immunol. 190: 1402-1406.
44. Kriesel, J. D., B. B. Jones, N. Matsunami, M. K. Patel, C. A. St Pierre, E. A. Kurt-Jones, R. W. Finberg, M. Leppert, and M. R. Hobbs. 2011. C21orf91 genotypes correlate with herpes simplex labialis (cold sore) frequency: description of a cold sore susceptibility gene. J. Infect. Dis. 204: 1654-1662.
45. Itzhaki, R., and M. Wozniak. 2008. Susceptibility to herpes simplex labialis conferred by the gene encoding apolipoprotein E. J. Infect. Dis. 198: 624-625, author reply 625-626.
46. Seppanen, M., S. Meri, I. L. Notkola, I. J. Seppala, E. Hiltunen-Back, H. Sarvas, M. Lappalainen, H. Valimaa, A. Palikhe, V. V. Valtonen, and M. L. Lokki. 2006. Subtly impaired humoral immunity predisposes to frequently recurring genital herpes simplex virus type 2 infection and herpetic neuralgia. J. Infect. Dis. 194: 571-578.
47. Vance, B. A., T. W. Huizinga, K. Wardwell, and P. M. Guyre. 1993. Binding of monomeric human IgG defines an expression polymorphism of Fc gamma RIII on large granular lymphocyte/natural killer cells. J. Immunol. 151: 6429-6439.
48. Varchetta, S., N. Gibelli, B. Oliviero, E. Nardini, R. Gennari, G. Gatti, L. S. Silva, L. Villani, E. Tagliabue, S. Ménard, et al. 2007. Elements related to heterogeneity of antibody-dependent cell cytotoxicity in patients under trastuzumab therapy for primary operable breast cancer overexpressing Her2. Cancer Res. 67: 11991-11999.
49. Hatjiharissi, E., L. Xu, D. D. Santos, Z. R. Hunter, B. T. Ciccarelli, S. Verselis, M. Modica, Y. Cao, R. J. Manning, X. Leleu, et al. 2007. Increased natural killer cell expression of CD16, augmented binding and ADCC activity to rituximab among individuals expressing the FcgammaRIIIa-158 V/V and V/F polymorphism. Blood 110: 2561-2564.
50. Shields, R. L., A. K. Namenuk, K. Hong, Y. G. Meng, J. Rae, J. Briggs, D. Xie, J. Lai, A. Stadlen, B. Li, et al. 2001. High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R. J. Biol. Chem. 276: 6591-6604.
51. Corrales-Aguilar, E., M. Trilling, K. Hunold, M. Fiedler, V. T. Le, H. Reinhard, K. Ehrhardt, E. Merce-Maldonado, E. Aliyev, A. Zimmermann, et al. 2014. Human cytomegalovirus Fcg binding proteins gp34 and gp68 antagonize Fcg receptors I, II and III. PLoS Pathog. 10: e1004131. doi:1004110.1001371/journal. ppat.1004131.
52. Bruhns, P., B. Iannascoli, P. England, D. A. Mancardi, N. Fernandez, S. Jorieux, and M. Daëron. 2009. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood 113: 3716-3725.
53. Erlich, K. S., and J. Mills. 1986. Passive immunotherapy for encephalitis caused by herpes simplex virus. Rev. Infect. Dis. 8(Suppl. 4): S439-S445.
54. LeBlanc, R. A., L. Pesnicak, M. Godleski, and S. E. Straus. 1999. Treatment of HSV-1 infection with immunoglobulin or acyclovir: comparison of their effects on viral spread, latency, and reactivation. Virology 262: 230-236.
55. Dalai, S. K., L. Pesnicak, G. F. Miller, and S. E. Straus. 2002. Prophylactic and therapeutic effects of human immunoglobulin on the pathobiology of HSV-1 infection, latency, and reactivation in mice. J. Neurovirol. 8: 35-44.
56. Sanna, P. P., A. De Logu, R. A. Williamson, Y. L. Hom, S. E. Straus, F. E. Bloom, and D. R. Burton. 1996. Protection of nude mice by passive immunization with a type-common human recombinant monoclonal antibody against HSV. Virology 215: 101-106.
57. Mayr, W. R., and D. Mickerts. 1970. [Human gamma globulin polymorphism. Calculation of its distribution in Vienna and its suitability in paternity cases]. Acta Biol. Med. Ger. 25: 473-482.
58. Namboodiri, A. M., and J. P. Pandey. 2011. Differential inhibition of trastuzumab-and cetuximab-induced cytotoxicity of cancer cells by immunoglobulin G1 expressing different GM allotypes. Clin. Exp. Immunol. 166: 361-365.
59. Dutertre, C. A., E. Bonnin-Gélizé, K. Pulford, D. Bourel, W. H. Fridman, and J. L. Teillaud. 2008. A novel subset of NK cells expressing high levels of inhibitory FcgammaRIIB modulating antibody-dependent function. J. Leukoc. Biol. 84: 1511-1520.
60. Ernst, L. K., D. Metes, R. B. Herberman, and P. A. Morel. 2002. Allelic polymorphisms in the FcgammaRIIC gene can influence its function on normal human natural killer cells. J. Mol. Med. 80: 248-257.
61. Maenaka, K., P. A. van der Merwe, D. I. Stuart, E. Y. Jones, and P. Sondermann. 2001. The human low affinity Fcgamma receptors IIa, IIb, and III bind IgG with fast kinetics and distinct thermodynamic properties. J. Biol. Chem. 276: 44898-44904.
62. Parsons, M. S., L. Wren, G. Isitman, M. Navis, I. Stratov, N. F. Bernard, and S. J. Kent. 2012. HIV infection abrogates the functional advantage of natural killer cells educated through KIR3DL1/HLA-Bw4 interactions to mediate anti-HIV antibody-dependent cellular cytotoxicity. J. Virol. 86: 4488-4495.
63. Parsons, M. S., L. Loh, S. Gooneratne, R. J. Center, and S. J. Kent. 2014. Role of education and differentiation in determining the potential of natural killer cells to respond to antibody-dependent stimulation. AIDS 28: 2781-2786.
64. Wu, Z., C. Sinzger, G. Frascaroli, J. Reichel, C. Bayer, L. Wang, R. Schirmbeck, and T. Mertens. 2013. Human cytomegalovirus-induced NKG2C(hi) CD57(hi) natural killer cells are effectors dependent on humoral antiviral immunity. J. Virol. 87: 7717-7725.
65. Costa-Garcia, M., A. Vera, M. Moraru, C. Vilches, M. López-Botet, and A. Muntasell. 2015. Antibody-mediated response of NKG2Cbright NK cells against human cytomegalovirus. J. Immunol. 194: 2715-2724.