Role of NKG2D, DNAM-1 and natural cytotoxicity receptors in cytotoxicity toward rhabdomyosarcoma cell lines mediated by resting and IL-15-activated human natural killer cells

Cancer Immunology, Immunotherapy

Volumn 64, Issue 5, 2015, Pages 573-583

  Boerman, Gerharda H ^a   van Ostaijen ten Dam, Monique M ^a   Kraal, Kathelijne C J M ^b   Santos, Susy J ^a   Ball, Lynne M ^a   Lankester, Arjan C ^a   Schilham, Marco W ^a   Egeler, R Maarten ^a,c   van Tol, Maarten J D ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Cytotoxicity; Immunotherapy; Natural killer cells; NK receptors; Rhabdomyosarcoma

Indexed keywords

DNAX ACCESSORY MOLECULE 1; HLA ANTIGEN CLASS 1; INTERLEUKIN 15; MYOGENIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; NECTIN 2; PROTEIN; UNCLASSIFIED DRUG; CD226 ANTIGEN; CYTOKINE; IL15 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; NCR1 PROTEIN, HUMAN; NCR3 PROTEIN, HUMAN; T LYMPHOCYTE ANTIGEN;

ANTIGEN BINDING; ARTICLE; CANCER CELL CULTURE; CANCER IMMUNOTHERAPY; CELL ISOLATION; CELL THERAPY; CHROMIUM RELEASE ASSAY; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RHABDOMYOSARCOMA; RHABDOMYOSARCOMA CELL LINE; SURVIVAL RATE; TARGET CELL; TUMOR BIOPSY; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; IMMUNOLOGY; TUMOR CELL LINE;

ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CELL LINE, TUMOR; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERLEUKIN-15; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RHABDOMYOSARCOMA;

EID: 84938424216     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-015-1657-9     Document Type: Article

References (35)

1. Pastore G, Peris-Bonet R, Carli M, Martinez-Garcia C, Sanchez de Toledo J, Steliarova-Foucher E (2006) Childhood soft tissue sarcomas incidence and survival in European children (1978–1997): report from the Automated Childhood Cancer Information System project. Eur J Cancer 42:2136–2149. doi:10.1016/j.ejca.2006.05.016
2. Oberlin O, Rey A, Lyden E, Bisogno G, Stevens MC, Meyer WH, Carli M, Anderson JR (2008) Prognostic factors in metastatic rhabdomyosarcomas: results of a pooled analysis from United States and European cooperative groups. J Clin Oncol 26:2384–2389. doi:10.1200/JCO.2007.14.7207
3. Davicioni E, Anderson MJ, Finckenstein FG et al (2009) Molecular classification of rhabdomyosarcoma—genotypic and phenotypic determinants of diagnosis: a report from the Children’s Oncology Group. Am J Pathol 174:550–564. doi:10.2353/ajpath.2009.080631
4. Fry TJ, Lankester AC (2008) Cancer immunotherapy: will expanding knowledge lead to success in pediatric oncology? Pediatr Clin North Am 55:147–167
5. Thiel U, Koscielniak E, Blaeschke F et al (2013) Allogeneic stem cell transplantation for patients with advanced rhabdomyosarcoma: a retrospective assessment. Br J Cancer 109:2523–2532. doi:10.1038/bjc.2013.630
6. Bryceson YT, Long EO (2008) Line of attack: NK cell specificity and integration of signals. Curr Opin Immunol 20:344–352. doi:10.1016/j.coi.2008.03.005
7. Moretta L, Bottino C, Pende D, Castriconi R, Mingari MC, Moretta A (2006) Surface NK receptors and their ligands on tumor cells. Semin Immunol 18:151–158
8. Parham P (2005) MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5:201–214. doi:10.1038/nri1570
9. Raulet DH (2003) Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 3:781–790. doi:10.1038/nri1199
10. Hayakawa Y, Smyth MJ (2006) NKG2D and cytotoxic effector function in tumor immune surveillance. Semin Immunol 18:176–185. doi:10.1016/j.smim.2006.03.005
11. Pende D, Bottino C, Castriconi R et al (2005) PVR (CD155) and Nectin-2 (CD112) as ligands of the human DNAM-1 (CD226) activating receptor: involvement in tumor cell lysis. Mol Immunol 42:463–469
12. Bryceson YT, March ME, Ljunggren HG, Long EO (2006) Activation, coactivation, and costimulation of resting human natural killer cells. Immunol Rev 214:73–91
13. Cho D, Shook DR, Shimasaki N, Chang YH, Fujisaki H, Campana D (2010) Cytotoxicity of activated natural killer cells against pediatric solid tumors. Clin Cancer Res 16:3901–3909. doi:10.1158/1078-0432.CCR-10-0735
14. Kuçi S, Rettinger E, Voss B et al (2010) Efficient lysis of rhabdomyosarcoma cells by cytokine-induced killer cells: implications for adoptive immunotherapy after allogeneic stem cell transplantation. Haematologica 95:1579–1586. doi:10.3324/haematol.2009.019885
15. Rettinger E, Meyer V, Kreyenberg H et al (2012) Cytotoxic capacity of IL-15-stimulated cytokine-induced killer cells against human acute myeloid leukemia and rhabdomyosarcoma in humanized preclinical mouse models. Front Oncol 2:32. doi:10.3389/fonc.2012.00032
16. Pahl JH, Ruslan SE, Kwappenberg KM, van Ostaijen-Ten Dam MM, van Tol MJ, Lankester AC, Schilham MW (2013) Antibody-dependent cell lysis by NK cells is preserved after sarcoma-induced inhibition of NK cell cytotoxicity. Cancer Immunol Immunother 62:1235–1247. doi:10.1007/s00262-013-1406-x
17. Verhoeven DHJ, de Hooge ASK, Mooiman ECK et al (2008) NK cells recognize and lyse Ewing sarcoma cells through NKG2D and DNAM-1 receptor dependent pathways. Mol Immunol 45:3917–3925. doi:10.1016/j.molimm.2008.06.016
18. Buddingh EP, Schilham MW, Ruslan SEN et al (2011) Chemotherapy-resistant osteosarcoma is highly susceptible to IL-15-activated allogeneic and autologous NK cells. Cancer Immunol Immunother 60:575–586. doi:10.1007/s00262-010-0965-3
19. Castriconi R, Dondero A, Corrias MV, Lanino E, Pende D, Moretta L, Bottino C, Moretta A (2004) Natural killer cell-mediated killing of freshly isolated neuroblastoma cells: critical role of DNAX accessory molecule-1-poliovirus receptor interaction. Cancer Res 64:9180–9184. doi:10.1158/0008-5472.CAN-04-2682
20. Sanchez-Correa B, Morgado S, Gayoso I et al (2011) Human NK cells in acute myeloid leukaemia patients: analysis of NK cell-activating receptors and their ligands. Cancer Immunol Immunother 60:1195–1205. doi:10.1007/s00262-011-1050-2
21. Carlsten M, Björkström NK, Norell H et al (2007) DNAX accessory molecule-1 mediated recognition of freshly isolated ovarian carcinoma by resting natural killer cells. Cancer Res 67:1317–1325. doi:10.1158/0008-5472.CAN-06-2264
22. Morgado S, Sanchez-Correa B, Casado JG, Duran E, Gayoso I, Labella F, Solana R, Tarazona R (2011) NK cell recognition and killing of melanoma cells is controlled by multiple activating receptor-ligand interactions. J Innate Immun 3:365–373. doi:10.1159/000328505
23. Rettinger E, Kuci S, Naumann I et al (2012) The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy 14:91–103. doi:10.3109/14653249.2011.613931
24. Holmes TD, El-Sherbiny YM, Davison A, Clough SL, Blair GE, Cook GP (2011) A human NK cell activation/inhibition threshold allows small changes in the target cell surface phenotype to dramatically alter susceptibility to NK cells. J Immunol 186:1538–1545. doi:10.4049/jimmunol.1000951
25. Oppenheim DE, Roberts SJ, Clarke SL, Filler R, Lewis JM, Tigelaar RE, Girardi M, Hayday AC (2005) Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 6:928–937. doi:10.1038/ni1239
26. Raffaghello L, Prigione I, Airoldi I et al (2004) Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia 6:558–568. doi:10.1593/neo.04316
27. Morandi F, Levreri I, Bocca P, Galleni B, Raffaghello L, Ferrone S, Prigione I, Pistoia V (2007) Human neuroblastoma cells trigger an immunosuppressive program in monocytes by stimulating soluble HLA-G release. Cancer Res 67:6433–6441. doi:10.1158/0008-5472.CAN-06-4588
28. Lang P, Pfeiffer M, Teltschik H-M et al (2011) Natural killer cell activity influences outcome after T cell depleted stem cell transplantation from matched unrelated and haploidentical donors. Best Pract Res Clin Haematol 24:403–411. doi:10.1016/j.beha.2011.04.009
29. Leung W, Iyengar R, Turner V, Lang P, Bader P, Conn P, Niethammer D, Handgretinger R (2004) Determinants of antileukemia effects of allogeneic NK cells. J Immunol 172:644–650
30. Perez-Martinez A, Leung W, Munoz E et al (2009) KIR–HLA receptor-ligand mismatch associated with a graft-versus-tumor effect in haploidentical stem cell transplantation for pediatric metastatic solid tumors. Pediatr Blood Cancer 53:120–124. doi:10.1002/pbc.21955
31. Pfeiffer MM, Feuchtinger T, Teltschik H-M, Schumm M, Müller I, Handgretinger R, Lang P (2010) Reconstitution of natural killer cell receptors influences natural killer activity and relapse rate after haploidentical transplantation of T- and B-cell depleted grafts in children. Haematologica 95:1381–1388. doi:10.3324/haematol.2009.021121
32. Koehl U, Sörensen J, Esser R et al (2004) IL-2 activated NK cell immunotherapy of three children after haploidentical stem cell transplantation. Blood Cells Mol Dis 33:261–266. doi:10.1016/j.bcmd.2004.08.013
33. Koehl U, Esser R, Zimmermann S et al (2005) Ex vivo expansion of highly purified NK cells for immunotherapy after haploidentical stem cell transplantation in children. Klin Pädiatr 217:345–350. doi:10.1055/s-2005-872520
34. Kanold J, Paillard C, Tchirkov A et al (2012) NK cell immunotherapy for high-risk neuroblastoma relapse after haploidentical HSCT. Pediatr Blood Cancer 59:739–742. doi:10.1002/pbc.24030
35. Miller JS, Soignier Y, Panoskaltsis-Mortari A et al (2005) Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105:3051–3057. doi:10.1182/blood-2004-07-2974