The role of interleukin-2, all-trans retinoic acid, and natural killer cells: surveillance mechanisms in anti-GD2 antibody therapy in neuroblastoma

Cancer Immunology, Immunotherapy

Volumn 67, Issue 4, 2018, Pages 615-626

  Nguyen, Rosa ^a   Houston, Jim ^a   Chan, Wing K ^b   Finkelstein, David ^a   Dyer, Michael A ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Anti GD2 antibody; IL 2; Missing self; Neuroblastoma; NK cells

Indexed keywords

ANTINEOPLASTIC MONOCLONAL ANTIBODY; CD159A ANTIGEN; CD3 ANTIGEN; CD56 ANTIGEN; CRABP1 PROTEIN; CRABP2 PROTEIN; CYTOCHROME P450 26A1; CYTOCHROME P450 26B1; DHRS3 PROTEIN; GANGLIOSIDE ANTIBODY; GANGLIOSIDE GD2; HLA B ANTIGEN; HLA C ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL1; LYMPHOCYTE ANTIGEN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MONOCLONAL ANTIBODY HU14.18K322A; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR NKG2D; PEPTIDES AND PROTEINS; RARB PROTEIN; RBP1 PROTEIN; RECOMBINANT INTERLEUKIN 2; RETINOIC ACID; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; GANGLIOSIDE; GANGLIOSIDE, GD2; INTERLEUKIN 2; MONOCLONAL ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN EXPRESSION; ARTICLE; CANCER IMMUNOTHERAPY; CHLA90 CELL LINE; CONTROLLED STUDY; DEGRANULATION; DISSOCIATED CELL CULTURE; DRUG EFFICACY; DRUG MECHANISM; FEASIBILITY STUDY; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; IMR-32 CELL LINE; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NB-1691 CELL LINE; NBL-S CELL LINE; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA; NEUROBLASTOMA CELL; NEUROBLASTOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; QUANTITATIVE ASSAY; SH-SY5Y CELL LINE; SK N JCI CELL LINE; SK N MM CELL LINE; SK N NAS CELL LINE; SK N NFI CELL LINE; SK-N-BE(2) CELL LINE; SK-N-SH CELL LINE; TUMOR CELL DESTRUCTION; TUMOR XENOGRAFT; IMMUNOLOGY; MULTIMODALITY CANCER THERAPY; PATHOLOGY; TUMOR CELL CULTURE;

ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; COMBINED MODALITY THERAPY; GANGLIOSIDES; HUMANS; INTERLEUKIN-2; KILLER CELLS, NATURAL; NEUROBLASTOMA; TRETINOIN; TUMOR CELLS, CULTURED;

EID: 85040375693     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-017-2108-6     Document Type: Article

References (40)

1. Zent CS, Chen JB, Kurten RC et al (2004) Alemtuzumab (CAMPATH 1H) does not kill chronic lymphocytic leukemia cells in serum free medium. Leuk Res 28:495–507. https://doi.org/10.1016/j.leukres.2003.09.011
2. Brentjens RJ, Davila ML, Riviere I et al (2013) CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 5:177ra38. https://doi.org/10.1126/scitranslmed.3005930
3. Larkin J, Chiarion-Sileni V, Gonzalez R et al (2015) Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 373:23–34. https://doi.org/10.1056/NEJMoa1504030
4. Slamon DJ, Leyland-Jones B, Shak S et al (2001) Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344:783–792. https://doi.org/10.1056/NEJM200103153441101
5. Hurwitz H, Fehrenbacher L, Novotny W et al (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350:2335–2342. https://doi.org/10.1056/NEJMoa032691
6. Yu AL, Gilman AL, Ozkaynak MF et al (2010) Anti-GD2 Antibody with GM-CSF, Interleukin-2, and Isotretinoin for Neuroblastoma. N Engl J Med 363:1324–1334. https://doi.org/10.1056/NEJMoa0911123
7. Schulz G, Cheresh DA, Varki NM et al (1984) Detection of ganglioside GD2 in tumor tissues and sera of neuroblastoma patients. Cancer Res 44:5914–5920
8. Janeway CA Jr, Travers P, Walport M et al (2001) Immunobiology: The Immune System in Health and Disease. 5th edn. New York: Garland Science. The destruction of antibody-coated pathogens via Fc receptors. http://www.ncbi.nlm.nih.gov/books/NBK27171/. Accessed 6 May 2017
9. Kärre K, Ljunggren HG, Piontek G, Kiessling R (1986) Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319:675–678. https://doi.org/10.1038/319675a0
10. Ruggeri L, Mancusi A, Capanni M et al (2007) Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood 110:433–440. https://doi.org/10.1182/blood-2006-07-038687
11. Henney CS, Kuribayashi K, Kern DE, Gillis S (1981) Interleukin-2 augments natural killer cell activity. Nature 291:335–338. https://doi.org/10.1038/291335a0
12. Villablanca JG, Khan AA, Avramis VI et al (1995) Phase I trial of 13-cis-retinoic acid in children with neuroblastoma following bone marrow transplantation. J Clin Oncol 13:894–901. https://doi.org/10.1200/JCO.1995.13.4.894
13. Stewart E, Shelat A, Bradley C et al (2015) Development and characterization of a human orthotopic neuroblastoma xenograft. Dev Biol 407:344–355. https://doi.org/10.1016/j.ydbio.2015.02.002
14. Downing JR, Wilson RK, Zhang J et al (2012) The pediatric cancer genome project. Nat Genet 44:619–622. https://doi.org/10.1038/ng.2287
15. Anders S, Pyl PT, Huber W (2015) HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169. https://doi.org/10.1093/bioinformatics/btu638
16. André P, Biassoni R, Colonna M et al (2001) New nomenclature for MHC receptors. Nat Immunol 2:661. https://doi.org/10.1038/90589
17. Brunner KT, Mauel J, Cerottini JC, Chapuis B (1968) Quantitative assay of the lytic action of immune lymphoid cells on 51-Cr-labelled allogeneic target cells in vitro; inhibition by isoantibody and by drugs. Immunology 14:181–196
18. Cederbrant K (2005) Natural killer cell assay. In: Vohr H-W (ed) Encyclopedic reference of immunotoxicology. Springer, Berlin, pp 469–472
19. Sorkin LS, Otto M, Baldwin WM et al (2010) Anti-GD2 with an FC point mutation reduces complement fixation and decreases antibody-induced allodynia. Pain 149:135–142. https://doi.org/10.1016/j.pain.2010.01.024
20. Alderson KL, Luangrath M, Elsenheimer MM et al (2013) Enhancement of the anti-melanoma response of Hu14.18K322A by αCD40 + CpG. Cancer Immunol Immunother 62:665–675. https://doi.org/10.1007/s00262-012-1372-8
21. Hank JA, Surfus J, Gan J et al (1994) Treatment of neuroblastoma patients with antiganglioside GD2 antibody plus interleukin-2 induces antibody-dependent cellular cytotoxicity against neuroblastoma detected in vitro. J Immunother Emphas Tumor Immunol 15:29–37
22. Rossi AR, Pericle F, Rashleigh S et al (1994) Lysis of neuroblastoma cell lines by human natural killer cells activated by interleukin-2 and interleukin-12. Blood 83:1323–1328
23. Brodin P, Lakshmikanth T, Johansson S et al (2009) The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood 113:2434–2441. https://doi.org/10.1182/blood-2008-05-156836
24. Joncker NT, Fernandez NC, Treiner E et al (2009) NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J Immunol 182:4572–4580. https://doi.org/10.4049/jimmunol.0803900
25. Howlander N, Noone A, Krapcho M et al (2011) SEER Cancer Statistics Review, 1975–2009. National Cancer Institute, Bethesda
26. Navid F, Sondel PM, Barfield R et al (2014) Phase I trial of a novel anti-GD2 monoclonal antibody, Hu14.18K322A, designed to decrease toxicity in children with refractory or recurrent neuroblastoma. J Clin Oncol 32:1445–1452. https://doi.org/10.1200/JCO.2013.50.4423
27. Grimm EA, Mazumder A, Zhang HZ, Rosenberg SA (1982) Lymphokine-activated killer cell phenomenon. Lysis of natural killer-resistant fresh solid tumor cells by interleukin 2-activated autologous human peripheral blood lymphocytes. J Exp Med 155:1823–1841
28. Hank JA, Robinson RR, Surfus J et al (1990) Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res 50:5234–5239
29. Ribeiro RC, Rill D, Roberson PK et al (1993) Continuous infusion of interleukin-2 in children with refractory malignancies. Cancer 72:623–628
30. Ladenstein R, Poetschger U, Gray J et al (2016) Toxicity and outcome of anti-GD2 antibody ch14.18/CHO in front-line, high-risk patients with neuroblastoma: final results of the phase III immunotherapy randomisation (HR-NBL1/SIOPEN trial). J Clin Oncol 34(15_suppl):Abstract 10500
31. Atkins MB, Gould JA, Allegretta M et al (1986) Phase I evaluation of recombinant interleukin-2 in patients with advanced malignant disease. J Clin Oncol 4:1380–1391. https://doi.org/10.1200/JCO.1986.4.9.1380
32. Lode H, Siebert N, Kietz S et al (2013) Long-term continuous infusion of anti-GD2 antibody CH14.18/CHO in relapsed/refractory neuroblastoma patients. J Immunother Cancer 1(1_suppl):Abstract P244
33. Delgado DC, Hank JA, Kolesar J et al (2010) Genotypes of NK Cell KIR Receptors, Their Ligands, and Fc Receptors in the Response of Neuroblastoma Patients to Hu14.18-IL2 Immunotherapy. Cancer Res 70:9554–9561. https://doi.org/10.1158/0008-5472.CAN-10-2211
34. Venstrom JM, Zheng J, Noor N et al (2009) KIR and HLA genotypes are associated with disease progression and survival following autologous hematopoietic stem cell transplantation for high-risk neuroblastoma. Clin Cancer Res 15:7330–7334. https://doi.org/10.1158/1078-0432.CCR-09-1720
35. Marsh SGE, Parham P, Barber LD (2000) The HLA factsbook. Academic Press, San Diego
36. Jin HJ, Nam HY, Bae YK et al (2010) GD2 expression is closely associated with neuronal differentiation of human umbilical cord blood-derived mesenchymal stem cells. Cell Mol Life Sci 67:1845–1858. https://doi.org/10.1007/s00018-010-0292-z
37. Zou Z, Nomura M, Takihara Y et al (1996) Isolation and characterization of retinoic acid-inducible cDNA clones in F9 cells: a novel cDNA family encodes cell surface proteins sharing partial homology with MHC class I molecules. J Biochem 119:319–328
38. Ho EL, Carayannopoulos LN, Poursine-Laurent J et al (2002) Costimulation of multiple NK cell activation receptors by NKG2D. J Immunol 169:3667–3675. https://doi.org/10.4049/jimmunol.169.7.3667
39. Reynolds CP, Kane DJ, Einhorn PA et al (1991) Response of neuroblastoma to retinoic acid in vitro and in vivo. Prog Clin Biol Res 366:203–211
40. Schug TT, Berry DC, Shaw NS et al (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129:723–733. https://doi.org/10.1016/j.cell.2007.02.050