The CD94/NKG2C+ NK-cell subset on the edge of innate and adaptive immunity to human cytomegalovirus infection

Seminars in Immunology

Volumn 26, Issue 2, 2014, Pages 145-151

  López Botet, Miguel ^a,b   Muntasell, Aura ^a   Vilches, Carlos ^c  

^a HOSPITAL DEL MAR   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

Author keywords

Cytomegalovirus; HLA; Human; Infection; NK cells; NKG2C

Indexed keywords

CD94 ANTIGEN; HOST FACTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY D;

ADAPTIVE IMMUNITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CYTOMEGALOVIRUS INFECTION; GENE DOSAGE; HOST CELL; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNE EVASION; IMMUNOCOMPROMISED PATIENT; INNATE IMMUNITY; NONHUMAN; PHENOTYPE; REVIEW; STEADY STATE; SURFACE PROPERTY; ANIMAL; CYTOMEGALOVIRUS; IMMUNOLOGY; METABOLISM; NATURAL KILLER CELL;

ADAPTIVE IMMUNITY; ANIMALS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D;

EID: 84897965082     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2014.03.002     Document Type: Review

References (98)

1. Mocarski E.S., Courcelle C.T. Cytomegaloviruses and their replication. Fields virology 2001, 2629-2673. Lippincott Williams & Wilkins, Philadelphia. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb (Eds.).
2. Crumpacker C.S. Cytomegalovirus. Mandell, Douglas, and Bennett' principles and practice of infectious diseases 2000, 1586-1599. Churchill Livingston, Philadelphia. G.L. Mandell, J.E. Bennett, R. Dolin (Eds.).
3. Stagno S. Cytomegalovirus. Infectious diseases of the fetus and newborn infant 2001, 389-424. W.B. Saunders Company, Philadelphia, PA. J.S. Remington, J.O. Klein (Eds.).
4. Pass R.F., Fowler K.B., Boppana S.B., Britt W.J., Stagno S. Congenital cytomegalovirus infection following first trimester maternal infection: symptoms at birth and outcome. J Clin Virol 2006, 35:216-220.
5. Fishman J.A. Infection in solid-organ transplant recipients. N Engl J Med 2007, 357:2601-2614.
6. Boeckh M., Ljungman P. How we treat cytomegalovirus in hematopoietic cell transplant recipients. Blood 2009, 113:5711-5719.
7. Elmaagacli A.H., Steckel N.K., Koldehoff M., Hegerfeldt Y., Trenschel R., Ditschkowski M., et al. Early human cytomegalovirus replication after transplantation is associated with a decreased relapse risk: evidence for a putative virus-versus-leukemia effect in acute myeloid leukemia patients. Blood 2011, 118:1402-1412.
8. Green M.L., Leisenring W.M., Xie H., Walter R.B., Mielcarek M., Sandmaier B.M., et al. CMV reactivation after allogeneic HCT and relapse risk: evidence for early protection in acute myeloid leukemia. Blood 2013, 122:1316-1324.
9. Pawelec G., Derhovanessian E. Role of CMV in immune senescence. Virus Res 2011, 157:175-179.
10. Romo N., Fitó M., Gumá M., Sala J., García C., Ramos R., et al. Association of atherosclerosis with expression of the LILRB1 receptor by human NK and T-cells supports the infectious burden hypothesis. Arterioscler Thromb Vasc Biol 2011, 31:2314-2321.
11. Waubant E., Mowry E.M., Krupp L., Chitnis T., Yeh E.A., Kuntz N., et al. Common viruses associated with lower pediatric multiple sclerosis risk. Neurology 2011, 76:1989-1995.
12. Biron C.A., Brossay L. NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol 2001, 13:458-464.
13. Tortorella D., Gewurz B.E., Furman M.H., Schust D.J., Ploegh H.L. Viral subversion of the immune system. Annu Rev Immunol 2000, 18:861-926.
14. López-Botet M., Angulo A., Gumá M. Natural killer cell receptors for major histocompatibility complex class I and related molecules in cytomegalovirus infection. Tissue Antigens 2004, 63:195-203.
15. Wilkinson G.W., Tomasec P., Stanton R.J., Armstrong M., Prod'homme V., Aicheler R., et al. Modulation of natural killer cells by human cytomegalovirus. J Clin Virol 2008, 41:206-212.
16. Eagle R.A., Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 2007, 7:737-744.
17. Raulet D.H., Gasser S., Gowen B.G., Deng W., Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol 2013, 31:413-441.
18. Chalupny N.J., Rein-Weston A., Dosch S., Cosman D. Down-regulation of the NKG2D ligand MICA by the human cytomegalovirus glycoprotein UL142. Biochem Biophys Res Commun 2006, 346:175-181.
19. Dunn C., Chalupny N.J., Sutherland C.L., Dosch S., Sivakumar P.V., Johnson D.C., et al. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med 2003, 197:1427-1439.
20. Stern-Ginossar N., Elefant N., Zimmermann A., Wolf D.G., Saleh N., Biton M., et al. Host immune system gene targeting by a viral miRNA. Science 2007, 317:376-381.
21. Jonjic S., Polic B., Krmpotic A. Viral inhibitors of NKG2D ligands: friends or foes of immune surveillance. Eur J Immunol 2008, 38:2952-2956.
22. Tomasec P., Wang E.C., Davison A.J., Vojtesek B., Armstrong M., Griffin C., et al. Downregulation of natural killer cell-activating ligand CD155 by human cytomegalovirus UL141. Nat Immunol 2005, 6:181-188.
23. Prod'homme V., Sugrue D.M., Stanton R.J., Nomoto A., Davies J., Rickards C.R., et al. Human cytomegalovirus UL141 promotes efficient downregulation of the natural killer cell activating ligand CD112. J Gen Virol 2010, 91:2034-2039.
24. Magri G., Muntasell A., Romo N., Sáez-Borderias A., Pende D., Geraghty D.E., et al. NKp46 and DNAM-1 NK-cell receptors drive the response to human cytomegalovirus-infected myeloid dendritic cells overcoming viral immune evasion strategies. Blood 2011, 117:848-856.
25. Smith W., Tomasec P., Aicheler R., Loewendorf A., Nemcovicova I., Wang E.C., et al. Human cytomegalovirus glycoprotein UL141 targets the TRAIL death receptors to thwart host innate antiviral defenses. Cell Host Microbe 2013, 13:324-335.
26. Moretta A., Bottino C., Vitale M., Pende D., Cantoni C., Mingari M.C., et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 2001, 19:197-223.
27. Brandt C.S., Baratin M., Yi E.C., Kennedy J., Gao Z., Fox B., et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exp Med 2009, 206:1495-1503.
28. Pogge von Strandmann P.E., Simhadri V.R., von Tresckow B., Sasse S., Reiners K.S., Hansen H.P., et al. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer, cells. Immunity 2007, 27:965-974.
29. Romo N., Magri G., Muntasell A., Heredia G., Baia D., Angulo A., et al. Natural killer cell-mediated response to human cytomegalovirus-infected macrophages is modulated by their functional polarization. J Leukoc Biol 2011, 90:717-726.
30. Moretta L., Bottino C., Pende D., Vitale M., Mingari M.C., Moretta A. Different checkpoints in human NK-cell activation. Trends Immunol 2004, 25:670-676.
31. López-Botet M., Bellón T. Natural killer cell activation and inhibition by receptors for MHC class I. Curr Opin Immunol 1999, 11:301-307.
32. Vilches C., Parham P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Immunol 2002, 20:217-251.
33. Lanier L.L. Natural killer cell receptor signaling. Curr Opin Immunol 2003, 15:308-314.
34. Colonna M., Navarro F., Bellón T., Llano M., García P., Samaridis J., et al. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J Exp Med 1997, 186:1809-1818.
35. Cosman D., Fanger N., Borges L., Kubin M., Chin W., Peterson L., et al. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 1997, 7:273-282.
36. Lanier L.L. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol 2008, 8:259-268.
37. Prod'homme V., Griffin C., Aicheler R.J., Wang E.C., McSharry B.P., Rickards C.R., et al. The human cytomegalovirus MHC class I homolog UL18 inhibits LIR-1+ but activates LIR-1- NK cells. J Immunol 2007, 178:4473-4481.
38. Llano M., Lee N., Navarro F., Garcia P., Albar J.P., Geraghty D.E., et al. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol 1998, 28:2854-2863.
39. Valés-Gómez M., Reyburn H.T., Erskine R.A., López-Botet M., Strominger J.L. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 1999, 18:4250-4260.
40. Petrie E.J., Clements C.S., Lin J., Sullivan L.C., Johnson D., Huyton T., et al. CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. J Exp Med 2008, 205:725-735.
41. Michaëlsson J., de Matos C.T., Achour A., Lanier L.L., Kärre K., Söderström K. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J Exp Med 2002, 196:1403-1414.
42. Ulbrecht M., Modrow S., Srivastava R., Peterson P.A., Weiss E.H. Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J Immunol 1998, 160:4375-4385.
43. Sullivan L.C., Clements C.S., Rossjohn J., Brooks A.G. The major histocompatibility complex class Ib molecule HLA-E at the interface between innate and adaptive immunity. Tissue Antigens 2008, 72:415-424.
44. Nattermann J., Nischalke H.D., Hofmeister V., Ahlenstiel G., Zimmermann H., Leifeld L., et al. The HLA-A2 restricted T cell epitope HCV core 35-44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. Am J Pathol 2005, 166:443-453.
45. Tomasec P., Braud V.M., Rickards C., Powell M.B., McSharry B.P., Gadola S., et al. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000, 287:1031.
46. Wang E.C., McSharry B., Retiere C., Tomasec P., Williams S., Borysiewicz L.K., et al. UL40-mediated NK evasion during productive infection with human cytomegalovirus. Proc Natl Acad Sci U S A 2002, 99:7570-7575.
47. Ulbrecht M., Martinozzi S., Grzeschik M., Hengel H., Ellwart J.W., Pla M., et al. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J Immunol 2000, 164:5019-5022.
48. Heatley S.L., Pietra G., Lin J., Widjaja J.M., Harpur C.M., Lester S., et al. Polymorphism in human cytomegalovirus UL40 impacts on recognition of HLA-E by natural killer cells. J Biol Chem 2013, 288:8679-8690.
49. Llano M., Gumá M., Ortega M., Angulo A., López-Botet M. Differential effects of US2, US6 and US11 human cytomegalovirus proteins on HLA class Ia and HLA-E expression: impact on target susceptibility to NK cell subsets. Eur J Immunol 2003, 33:2744-2754.
50. Parham P. MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 2005, 5:201-214.
51. Ameres S., Mautner J., Schlott F., Neuenhahn M., Busch D.H., Plachter B., et al. Presentation of an immunodominant immediate-early CD8+ T cell epitope resists human cytomegalovirus immunoevasion. PLoS Pathog 2013, 9:e1003383.
52. Barel M.T., Pizzato N., Le B.P., Wiertz E.J., Lenfant F. Subtle sequence variation among MHC class I locus products greatly influences sensitivity to HCMV US2- and US11-mediated degradation. Int Immunol 2006, 18:173-182.
53. Moretta L., Moretta A. Killer immunoglobulin-like receptors. Curr Opin Immunol 2004, 16:626-633.
54. Lanier L.L. NK cell recognition. Annu Rev Immunol 2005, 23:225-274.
55. Arase H., Mocarski E.S., Campbell A.E., Hill A.B., Lanier L.L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002, 296:1323-1326.
56. Smith H.R., Heusel J.W., Mehta I.K., Kim S., Dorner B.G., Naidenko O.V., et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci U S A 2002, 99:8826-8831.
57. Lanier L.L. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 2008, 9:495-502.
58. Elliott J.M., Yokoyama W.M. Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol 2011, 32:364-372.
59. Gumá M., Angulo A., Vilches C., Gómez-Lozano N., Malats N., López-Botet M. Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 2004, 104:3664-3671.
60. Monsivais-Urenda A., Noyola-Cherpitel D., Hernández-Salinas A., García-Sepúlveda C., Romo N., Baranda L., et al. Influence of human cytomegalovirus infection on the NK cell receptor repertoire in children. Eur J Immunol 2010, 40:1418-1427.
61. Béziat V., Liu L., Malmberg J.A., Ivarsson M.A., Sohlberg E., Björklund A.T., et al. NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 2013, 121:2678-2688.
62. Noyola D.E., Fortuny C., Muntasell A., Noguera-Julian A., Muñoz-Almagro C., Alarcón A., et al. Influence of congenital human cytomegalovirus infection and the NKG2C genotype on NK-cell subset distribution in children. Eur J Immunol 2012, 42:3256-3266.
63. Muntasell A., López-Montañés M., Vera A., Heredia G., Romo N., Peñafiel J., et al. NKG2C zygosity influences CD94/NKG2C receptor function and the NK-cell compartment redistribution in response to human cytomegalovirus. Eur J Immunol 2013, 43:3268-3278.
64. Djaoud Z., David G., Bressollette C., Willem C., Rettman P., Gagne K., et al. Amplified NKG2C+ NK cells in cytomegalovirus (CMV) infection preferentially express killer cell Ig-like receptor 2DL: functional impact in controlling CMV-infected dendritic cells. J Immunol 2013, 191:2708-2716.
65. Bjorkström N.K., Lindgren T., Stoltz M., Fauriat C., Braun M., Evander M., et al. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med 2011, 208:13-21.
66. Gumá M., Cabrera C., Erkizia I., Bofill M., Clotet B., Ruiz L., et al. Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94/NKG2C receptor in aviremic HIV-1-positive patients. J Infect Dis 2006, 194:38-41.
67. Mela C.M., Goodier M.R. The contribution of cytomegalovirus to changes in NK cell receptor expression in HIV-1-infected individuals. J Infect Dis 2007, 195:158-159.
68. Brunetta E., Fogli M., Varchetta S., Bozzo L., Hudspeth K.L., Marcenaro E., et al. Chronic HIV-1 viremia reverses NKG2A/NKG2C ratio on natural killer cells in patients with human cytomegalovirus co-infection. AIDS 2010, 24:27-34.
69. Petitdemange C., Becquart P., Wauquier N., Beziat V., Debré P., Leroy E.M., et al. Unconventional repertoire profile is imprinted during acute chikungunya infection for natural killer cells polarization toward cytotoxicity. PLoS Pathog 2011, 7:e1002268.
70. Béziat V., Dalgard O., Asselah T., Halfon P., Bedossa P., Boudifa A., et al. CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur J Immunol 2012, 42:447-457.
71. Saghafian-Hedengren S., Söhlberg E., Theorell J., Carvalho-Queiroz C., Nagy N., Persson J.O., et al. Epstein-barr virus coinfection in children boosts cytomegalovirus-induced differentiation of natural killer cells. J Virol 2013, 87:13446-13455.
72. Muntasell A., Vilches C., Angulo A., López-Botet M. Adaptive reconfiguration of the human NK-cell compartment in response to cytomegalovirus: a different perspective of the host-pathogen interaction. Eur J Immunol 2013, 43:1133-1141.
73. Waggoner S.N., Cornberg M., Selin L.K., Welsh R.M. Natural killer cells act as rheostats modulating antiviral T cells. Nature 2011, 481:394-398.
74. Kuijpers T.W., Baars P.A., Dantin C., van den Burg M., van Lier R.A., Roosnek E. Human NK cells can control CMV infection in the absence of T cells. Blood 2008, 112:914-915.
75. López-Vergès S., Milush J.M., Schwartz B.S., Pando M.J., Jarjoura J., York V.A., et al. Expansion of a unique CD57NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci U S A 2011, 108:14725-14732.
76. Della Chiesa M., Falco M., Podesta M., Locatelli F., Moretta L., Frassoni F., et al. Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus?. Blood 2012, 119:399-410.
77. Foley B., Cooley S., Verneris M.R., Curtsinger J., Luo X., Waller E.K., et al. Human cytomegalovirus (CMV)-induced memory-like NKG2C+ NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J Immunol 2012, 189:5082-5088.
78. Foley B., Cooley S., Verneris M.R., Pitt M., Curtsinger J., Luo X., et al. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 2012, 119:2665-2674.
79. Bengner M., Béziat V., Ernerudh J., Nilsson B.O., Lofgren S., Wikby A., et al. Independent skewing of the T cell and NK cell compartments associated with cytomegalovirus infection suggests division of labor between innate and adaptive immunity. Age 2013, (Ahead of print).
80. Miyashita R., Tsuchiya N., Hikami K., Kuroki K., Fukazawa T., Bijl M., et al. Molecular genetic analyses of human NKG2C (KLRC2) gene deletion. Int Immunol 2004, 16:163-168.
81. Moraru M., Cisneros E., Gómez-Lozano N., de Pablo R., Portero F., Cañizares M., et al. 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 2012, 188:4412-4420.
82. Rangel-Ramírez V.V., García-Sepúlveda C.A., Escalante-Padron F., Pérez-González L.F., Rangel-Castilla A., Aranda-Romo S., et al. NKG2C gene deletion in the Mexican population and lack of association to respiratory viral infections. Int J Immunogenet 2013, 41:126-130.
83. Sun J.C., Beilke J.N., Lanier L.L. Adaptive immune features of natural killer cells. Nature 2009, 457:557-561.
84. Vivier E., Raulet D.H., Moretta A., Caligiuri M.A., Zitvogel L., Lanier L.L., et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011, 331:44-49.
85. Gumá M., Busch L.K., Salazar-Fontana L.I., Bellosillo B., Morte C., García P., et al. The CD94/NKG2C killer lectin-like receptor constitutes an alternative activation pathway for a subset of CD8+ T cells. Eur J Immunol 2005, 35:2071-2080.
86. Gumá M., Budt M., Sáez A., Brckalo T., Hengel H., Angulo A., et al. Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 2006, 107:3624-3631.
87. Zhang T., Scott J.M., Hwang I., Kim S. Cutting edge: antibody-dependent memory-like NK cells distinguished by FcRgamma deficiency. J Immunol 2013, 190:1402-1406.
88. Wu Z., Sinzger C., Frascaroli G., Reichel J., Bayer C., Wang L., et al. Human cytomegalovirus-induced NKG2C(hi) CD57(hi) natural killer cells are effectors dependent on humoral antiviral immunity. J Virol 2013, 87:7717-7725.
89. Stern M., Hadaya K., Honger G., Martin P.Y., Steiger J., Hess C., et al. Telomeric rather than centromeric activating KIR genes protect from cytomegalovirus infection after kidney transplantation. Am J Transplant 2011, 11:1302-1307.
90. Della-Chiesa M., Falco M., Bertaina A., Muccio L., Alicata C., Frassoni F., et al. Human cytomegalovirus infection promotes rapid maturation of NK cells expressing activating killer Iglike receptor in patients transplanted with NKG2C/umbilical cord blood. J Immunol 2014, 192:1471-1479.
91. White D.W., Suzanne B.R., Barton E.S. Immune modulation during latent herpesvirus infection. Immunol Rev 2012, 245:189-208.
92. Thomas R., Low H.Z., Kniesch K., Jacobs R., Schmidt R.E., Witte T. NKG2C deletion is a risk factor of HIV infection. AIDS Res Hum Retroviruses 2012, 28:844-851.
93. Goodier M.R., Mela C.M., Steel A., Gazzard B., Bower M., Gotch F. NKG2C+ NK cells are enriched in AIDS patients with advanced-stage Kaposi's sarcoma. J Virol 2007, 81:430-433.
94. Velardi A., Ruggeri L., Mancusi A. Killer-cell immunoglobulin-like receptors reactivity and outcome of stem cell transplant. Curr Opin Hematol 2012, 19:319-323.
95. Moretta L., Locatelli F., Pende D., Marcenaro E., Mingari M.C., Moretta A. Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood 2011, 117:764-771.
96. Kreutzman A., Ladell K., Koechel C., Gostick E., Ekblom M., Stenke L., et al. Expansion of highly differentiated CD8+ T-cells or NK-cells in patients treated with dasatinib is associated with cytomegalovirus reactivation. Leukemia 2011, 25:1587-1597.
97. Kreutzman A., Jaatinen T., Greco D., Vakkila E., Richter J., Ekblom M., et al. Killer-cell immunoglobulin-like receptor gene profile predicts good molecular response to dasatinib therapy in chronic myeloid leukemia. Exp Hematol 2012, 40:906-913.
98. Martínez-Rodríguez J.E., Munné-Collado J., Rasal R., Cuadrado E., Roig L., Ois A., et al. Expansion of the NKG2C+ natural killer-cell subset is associated with high-risk carotid atherosclerotic plaques in seropositive patients for human cytomegalovirus. Arterioscler Thromb Vasc Biol 2013, 33:2653-2659.