Characterization of IFNγ-producing natural killer cells induced by cytomegalovirus reactivation after haploidentical hematopoietic stem cell transplantation

Oncotarget

Volumn 8, Issue 1, 2017, Pages 51-63

  Jin, Fengyan ^a   Lin, Hai ^a   Gao, Sujun ^a   Wang, Hengxiang ^b   Yan, Hongmin ^b   Guo, Jinglong ^a   Hu, Zheng ^a   Jin, Chunhui ^a   Wang, Yongqi ^b   Wang, Zhidong ^b   Zhao, Yangzhi ^a   Liu, Yu ^a   Zheng, Xiaoli ^b   Tan, Yehui ^a   Li, Wei ^a   Dai, Yun ^a   Yang, Yanping ^a  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b AIR FORCE GENERAL HOSPITAL   (China)

Author keywords

Cytomegalovirus; IFN ; KIR; NK cells; NKG2C; Pathology section

Indexed keywords

CD56 ANTIGEN; GAMMA INTERFERON; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY 2A; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY 2C; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; INWARDLY RECTIFYING POTASSIUM CHANNEL;

ADOLESCENT; ADULT; ANTIVIRAL THERAPY; ARTICLE; CELL DENSITY; CELL EXPANSION; CELL FUNCTION; CELL MATURATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; FEMALE; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; LEUKEMIA RELAPSE; MALE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; VIRUS DETECTION; VIRUS REACTIVATION; ADVERSE EVENT; ALLOTRANSPLANTATION; BIOSYNTHESIS; GENETICS; IMMUNOLOGY; K-562 CELL LINE; METABOLISM; MIDDLE AGED; PRESCHOOL CHILD; TIME FACTOR; VIRUS ACTIVATION; YOUNG ADULT;

ADOLESCENT; ADULT; BIOMARKERS; CHILD; CHILD, PRESCHOOL; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INTERFERON-GAMMA; K562 CELLS; KILLER CELLS, NATURAL; MALE; MIDDLE AGED; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; PHENOTYPE; POTASSIUM CHANNELS, INWARDLY RECTIFYING; TIME FACTORS; TRANSPLANTATION, HOMOLOGOUS; VIRUS ACTIVATION; YOUNG ADULT;

EID: 85009787179     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.13916     Document Type: Article

References (42)

1. Saber W, Opie S, Rizzo JD, Zhang M-J, Horowitz MM and Schriber J. Outcomes after matched unrelated donor versus identical sibling hematopoietic cell transplantation in adults with acute myelogenous leukemia. Blood. 2012; 119:3908-3916.
2. Parmesar K and Raj K. Haploidentical stem cell transplantation in adult haematological malignancies. Adv Hematol. 2016; 2016:3905907.
3. Moretta A, Bottino C, Vitale M, Pende D, Biassoni R, Mingari MC and Moretta L. Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol. 1996; 14:619-648.
4. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R and Moretta L. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol. 2001; 19:197-223.
5. Lanier LL. Evolutionary struggles between NK cells and viruses. Nat Rev Immunol. 2008; 8: 259-268.
6. Vivier E, Tomasello E, Baratin M, Walzer T and Ugolini S. Functions of natural killer cells. Nat Immunol. 2008; 9:503-510.
7. Long EO. Signal sequences stop killer cells. Nature. 1998; 391:740-743.
8. Rölle A Pollmann J, Ewen E-M, Le VTK, Halenius A, Hengel H and Cerwenka A. IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+ NK cell expansion. J Clin Invest. 2014; 124:5305-5316.
9. Béziat V, Liu LL, Malmberg JA, Ivarsson MA, Sohlberg E, Björklund AT, Retière C, Sverremark-Ekström E, Traherne J, Ljungman P, Schaffer M, Price DA, Trowsdale J, 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.
10. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, Lopez-Vergès S, Lanier LL, Weisdorf D and Miller JS. Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood. 2012; 119:2665-2674.
11. Foley B, Cooley S, Verneris MR, Curtsinger J, Luo X, Waller EK, Anasetti C, Weisdorf D and Miller JS. 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.
12. Charoudeh HN, Terszowski G, Czaja K, Gonzalez A, Schmitter K and Stern M. Modulation of the natural killer cell KIR repertoire by cytomegalovirus infection. Eur J Immunol. 2013; 43:480-487.
13. Monsiváis-Urenda A, Noyola-Cherpitel D, Hernández-Salinas A, García-Sepúlveda C, Romo N, Baranda L, López-Botet M and González-Amaro R. Influence of human cytomegalovirus infection on the NK cell receptor repertoire in children. Eur J Immunol. 2010; 40:1418-1427.
14. Biron CA. Expansion, maintenance, and memory in NK and T cells during viral infections: responding to pressures for defense and regulation. PLoS Pathog. 2010; 6:e1000816.
15. Sun JC, Beilke JN and Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009; 457:557-561.
16. Foley B, Cooley S, Verneris MR, Curtsinger J, Luo X, Waller EK, Weisdorf DJ and Miller JS. NK cell education after allogeneic transplantation: dissociation between recovery of cytokine-producing and cytotoxic functions. Blood. 2011; 118:2784-2792.
17. Foley B, Felices M, Cichocki F, Cooley S, Verneris MR and Miller JS. The biology of NK cells and their receptors affects clinical outcomes after hematopoietic cell transplantation (HCT). Immunol Rev. 2014; 258:45-63.
18. Jacobs R, Hintzen G, Kemper A, Beul K, Kempf S, Behrens G, Sykora KW and Schmidt RE. CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur J Immunol. 2001; 31:3121-3127.
19. Robertson MJ, Manley TJ, Donahue C, Levine H and Ritz J. Costimulatory signals are required for optimal proliferation of human natural killer cells. J Immunol. 1993; 150:1705-1714.
20. Malhotra1 A and Shanker A. NK cells: immune crosstalk and therapeutic implications. Immunotherapy. 2011; 3:1143-1166.
21. Babic M, Krmpotic A and Jonjic S. All is fair in virus-host interactions: NK cells and cytomegalovirus. Trends Mol Med. 2011; 17:677-685.
22. Foley B, Cooley S, Verneris MR, Curtsinger J, Luo X, Waller EK, Weisdorf DJ and Miller JS. NK cell education after allogeneic transplantation: dissociation between recovery of cytokine-producing and cytotoxic functions. Blood. 2011; 118:2784-2792.
23. Boyington JC and Sun PD. A structural perspective on MHC class I recognition by killer cell immunoglobulin-like receptors. Mol Immunol. 2002; 38:1007-1021.
24. Cooley S, Weisdorf DJ, Guethlein LA, Klein JP, Wang T, Marsh SG, Spellman S, Haagenson MD, Saeturn K, Ladner M, Trachtenberg E, Parham P and Miller JS. Donor killer cell Ig-like receptor B haplotypes, recipient HLA-C1, and HLA-C mismatch enhance the clinical benefit of unrelated transplantation for acute myelogenous leukemia. J Immunol. 2014; 19:4592-600.
25. Gumperz JE, Litwin V, Phillips JH, Lanier LL and Parham P. The Bw4 public epitope of HLA-B molecules confers reactivity with natural killer cell clones that express NKB1, a putative HLA receptor. J Exp Med. 1995; 181:1133-44.
26. Gumperz JE, Barber LD, Valiante NM, Percival L, Phillips JH, Lanier LL and Parham P. Conserved and variable residues within the Bw4 motif of HLA-B make separable contributions to recognition by the NKB1 killer cellinhibitory receptor. J Immunol. 1997; 158:5237-5241.
27. Kheav VD, Busson M, Scieux C, Peffault de Latour R, Maki G, Haas P, Mazeron MC, Carmagnat M, Masson E, Xhaard A, Robin M, Ribaud P, Dulphy N, et al. Favorable impact of natural killer cell reconstitution on chronic graft-versus-host disease and cytomegalovirus reactivation after allogeneic hematopoietic stem cell transplantation. Haematologica. 2014; 99:1860-1867.
28. Sun JC, Beilke JN and Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009; 457:557-561.
29. Braud VM, Allan DS, O'Callaghan CA, Söderström K, D'Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, Lanier LL and McMichael AJ. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998; 391:795-799
30. Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP, Gadola S, Cerundolo V, Borysiewicz LK, McMichael AJ and Wilkinson GW. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science. 2000; 287:1031.
31. Llano M, Gumá M, Ortega M, Angulo A and 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.
32. Björkström NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, Michaëlsson J, Malmberg KJ, Klingström J, Ahlm C and Ljunggren HG. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med. 2011; 208:13-21.
33. Szomolanyi-Tsuda E, Liang X, Welsh RM, Kurt-Jones EA and Finberg RW. Role for TLR2 in NK cell-mediated control of murine cytomegalovirus in vivo. J Virol 2006; 80: 4286-4291.
34. Hossain MS, Ramachandiran S, Gewirtz AT and Waller EK. Recombinant TLR5 agonist CBLB502 promotes NK cellmediated anti-CMV immunity in mice. PLOS ONE 2014; 9:e96165.
35. Béziat V, Dalgard O, Asselah T, Halfon P, Bedossa P, Boudifa A, Hervier B, Theodorou I, Martinot M, Debré P, Björkström NK, Malmberg K-J, Marcellin P, et al. CMV drives clonal expansion of NKG2C1 NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur J Immunol. 2012; 42:447-457.
36. Djaoud Z, David G, Bressollette C, Willem C, Rettman P, Gagne K, Legrand N, Mehlal S, Cesbron A, Imbert-Marcille BM and Retière C. 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.
37. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ and Schreiber RD. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001; 410:1107-1111.
38. Biron CA, Nguyen KB, Pien GC, Cousens LP and Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol. 1999; 17:189-220.
39. Yawata M, Yawata N, Draghi M, Partheniou F, Little AM and Parham P. MHC class I-specific inhibitory receptors and their ligands structure diverse human NK-cell repertoires toward a balance of missing self-response. Blood. 2008; 112:2369-2380.
40. Stern M, de Angelis C, Urbani E, Mancusi A, Aversa F, Velardi A and Ruggeri L. Natural killer-cell KIR repertoire reconstitution after haploidentical SCT. Bone Marrow Transplant. 2010; 45:1607-1610.
41. Wang Y, Chang YJ, Xu LP, Liu KY, Liu DH, Zhang XH, Chen H, Han W, Chen YH, Wang FR, Wang JZ, Chen Y, Yan CH, et al. Who is the best donor for a related HLA haplotype-mismatched transplant? Blood. 2014; 124:843-850.
42. Chen DF, Prasad VK, Broadwater G, Reinsmoen NL, DeOliveira A, Clark A, Sullivan KM, Chute JP, Horwitz ME, Gasparetto C, Long GD, Yang Y, Chao NJ, et al. Differential impact of inhibitory and activating Killer Ig-Like Receptors (KIR) on high-risk patients with myeloid and lymphoid malignancies undergoing reduced intensity transplantation from haploidentical related donors. Bone Marrow Transplant. 2012; 47:817-823.