Increasing the clinical efficacy of NK and antibody-mediated cancer immunotherapy: Potential predictors of successful clinical outcome based on observations in high-risk neuroblastoma

Frontiers in Pharmacology

Volumn 3 MAY, Issue , 2012, Pages

  Koehn, Tony A ^a   Trimble, Lori L ^a   Alderson, Kory L ^a   Erbe, Amy K ^a   McDowell, Kimberly A ^a   Grzywacz, Bartosz ^b   Hank, Jacquelyn A ^a,b   Sondel, Paul M ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

ADCC; FcR; IL2; Immunocytokine; KIR; mAb; Neuroblastoma

Indexed keywords

ANTINEOPLASTIC AGENT; CETUXIMAB; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HU 14.18 IL2 IC; RITUXIMAB; TRASTUZUMAB; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ALLERGIC REACTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER IMMUNOTHERAPY; CAPILLARY LEAK SYNDROME; COMPUTER ASSISTED TOMOGRAPHY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXICITY; DRUG EFFICACY; HIGH RISK PATIENT; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NATURAL KILLER CELL; NEUROBLASTOMA; NONHODGKIN LYMPHOMA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PAIN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84866039189     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00091     Document Type: Article

References (72)

1. Adams, G. P., and Weiner, L. M. (2005). Monoclonal antibody therapy of cancer. Nat. Biotechnol. 23, 1147-1157.
2. Alvarez-Rueda, N., Desselle, A., Cochonneau, D., Chaumette, T., Clemenceau, B., Leprieur, S., Bougras, G., Supiot, S., Mussini, J. M., Barbet, J., Saba, J., Paris, F., Aubry, J., and Birkle, S. (2011). A monoclonal antibody to O-acetyl-GD2 ganglioside and not to GD2 shows potent anti-tumor activity without peripheral nervous system crossreactivity. PLoS ONE 6, e25220. doi:10.1371/journal.pone.0025220
3. Alves, L. G., Rajalingam, R., and Canavez, F. (2009). A novel real-time PCR method for KIR genotyping. Tissue Antigens 73, 188-191.
4. Bachanova, V., Burns, L. J., Mckenna, D. H., Curtsinger, J., Panoskaltsis-Mortari, A., Lindgren, B. R., Cooley, S., Weisdorf, D., and Miller, J. S. (2010). Allogeneic natural killer cells for refractory lymphoma. Cancer Immunol. Immunother. 59, 1739-1744.
5. Basham, T. Y., Race, E. R., Campbell, M. J., Reid, T. R., Levy, R., and Merigan, T. C. (1988). Synergistic antitumor activity with IFN and monoclonal anti-idiotype for murine B cell lymphoma. Mechanism of action. J. Immunol. 141, 2855-2860.
6. Becknell,B.,and Caligiuri,M. A. (2008). Natural killer cells in innate immunity and cancer. J. Immunother. 31, 685-692.
7. Biron, C. A., Nguyen, K. B., Pien, G. C., Cousens, L. P., and Salazar-Mather, T. P. (1999). Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17, 189-220.
8. Borgerding, A., Hasenkamp, J., Engelke, M., Burkhart, N., Trümper, L., Wienands, J., and Glass, B. (2010). B-lymphoma cells escape rituximab-triggered elimination by NK cells through increased HLA class I expression. Exp. Hematol. 38, 213-221.
9. Buhtoiarov, I. N., Neal, Z. C., Gan, J., Buhtoiarova, T. N., Patankar, M. S., Gubbels, J. A., Hank, J. A., Yamane, B., Rakhmilevich, A. L., Reisfeld, R. A., Gillies, S. D., and Sondel, P. M. (2011). Differential internalization of hu14.18-IL2 immunocytokine by NK and tumor cell: impact on conjugation, cytotoxicity, and targeting. J. Leukoc. Biol. 89, 625-638.
10. Cartron, G., Dacheux, L., Salles, G., Solal-Celigny, P., Bardos, P., Colombat, P., and Watier, H. (2002). Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 99, 754-758.
11. Clynes, R. A., Towers, T. L., Presta, L. G., and Ravetch, J. V. (2000). Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med. 6, 443-446.
12. Delgado, D. C., Hank, J. A., Kolesar, J., Lorentzen, D., Gan, J., Seo, S., Kim, K., Shusterman, S., Gillies, S. D., Reisfeld, R. A., Yang, R., Gadbaw, B., Desantes, K. B., London, W. B., Seeger, R. C., Maris, J. M., and Sondel, P. M. (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.
13. Dougan, M., and Dranoff, G. (2009). Immune therapy for cancer. Annu. Rev. Immunol. 27, 83-117.
14. Farag, S. S., and Caligiuri, M. A. (2006). Human natural killer cell development and biology. Blood Rev. 20, 123-137.
15. Farag, S. S.,Vandeusen, J. B., Fehniger, T. A., and Caligiuri, M. A. (2003). Biology and clinical impact of human natural killer cells. Int. J. Hematol. 78, 7-17.
16. Geller, M. A., Cooley, S., Judson, P. L., Ghebre, R., Carson, L. F., Argenta, P. A., Jonson, A. L., Panoskaltsis-Mortari, A., Curtsinger, J., Mckenna, D., Dusenbery, K., Bliss, R., Downs, L. S., and Miller, J. S. (2011). A phase II study of allogeneic natural killer cell therapy to treat patients with recurrent ovarian and breast cancer. Cytotherapy 13, 98-107.
17. Gillies, S. D., Lan, Y., Williams, S., Carr, F., Forman, S., Raubitschek, A., and Lo, K. M. (2005). An anti-CD20-IL-2 immunocytokine is highly efficacious in a SCID mouse model of established human B lymphoma. Blood 105, 3972-3978.
18. Gillies, S. D., Reilly, E. B., Lo, K. M., and Reisfeld,R. A. (1992). Antibodytargeted interleukin 2 stimulates T-cell killing of autologous tumor cells. Proc. Natl. Acad. Sci. U.S.A. 89, 1428-1432.
19. Gubbels,J. A.,Gadbaw,B.,Buhtoiarov,I. N., Horibata, S., Kapur, A. K., Patel, D., Hank, J. A., Gillies, S. D., Sondel, P. M., Patankar, M. S., and Connor,J. (2011).Ab-IL2 fusion proteins mediate NK cell immune synapse formation by polarizing CD25 to the target cell-effector cell interface. Cancer Immunol. Immunother. 60, 1789-1800.
20. Hank, J. A., Albertini, M. R., Schiller, J., and Sondel, P. M. (1993). Activation of multiple effector mechanisms to enhance tumor immunotherapy. J. Immunother. Emphasis Tumor Immunol. 14, 329-335.
21. Hank, J. A., Kohler, P. C., Weil-Hillman, G., Rosenthal, N., Moore, K. H., Storer, B., Minkoff, D., Bradshaw, J., Bechhofer, R., and Sondel, P. M. (1988). In vivo induction of the lymphokine-activated killer phenomenon: interleukin 2-dependent human non-major histocompatibility complex-restricted cytotoxicity generated in vivo during administration of human recombinant interleukin 2. Cancer Res. 48, 1965-1971.
22. Hank, J. A., Robinson, R. R., Surfus, J., Mueller, B. M., Reisfeld, R. A., Cheung, N. K., and Sondel, P. M. (1990). Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res. 50, 5234-5239.
23. Hong, H. A., Loubser, A. S., De Assis Rosa, D., Naranbhai, V., Carr, W., Paximadis, M., Lewis, D. A., Tiemessen, C. T., and Gray, C. M. (2011). Killer-cell immunoglobulinlike receptor genotyping and HLA killer-cell immunoglobulin-like receptor-ligand identification by real-time polymerase chain reaction. Tissue Antigens 78, 185-194.
24. Hsu, K. C., Keever-Taylor, C. A., Wilton, A., Pinto, C., Heller, G., Arkun, K., O'Reilly, R. J., Horowitz, M. M., and Dupont, B. (2005). Improved outcome in HLA-identical sibling hematopoietic stem-cell transplantation for acute myelogenous leukemia predicted by KIR and HLA genotypes. Blood 105, 4878-4884.
25. Huenecke, S., Zimmermann, S. Y., Kloess, S., Esser, R., Brinkmann, A., Tramsen, L., Koenig, M., Erben, S., Seidl, C., Tonn, T., Eggert, A., Schramm, A., Bader, P., Klingebiel, T., Lehrnbecher, T., Passweg, J. R., Soerensen, J., Schwabe, D., and Koehl,U. (2010). IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16-subpopulations and in vivo influence after haploidentical NK cell infusion. J. Immunother. 33, 200-210.
26. Jefferis, R. (2007). Antibody therapeutics: isotype and glycoform selection. Expert Opin. Biol. Ther. 7, 1401-1413.
27. Johnson, E., Dean, S. M., and Sondel, P. M. (2007). Antibody-based immunotherapy in high-risk neuroblastoma. Expert Rev. Mol. Med. 9, 1-21.
28. Karapetis, C. S., Khambata-Ford, S., Jonker, D. J., O'Callaghan, C. J., Tu, D., Tebbutt, N. C., Simes, R. J., Chalchal, H., Shapiro, J. D., Robitaille, S., Price, T. J., Shepherd, L., Au, H. J., Langer, C., Moore, M. J., and Zalcberg, J. R. (2008). K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N.Engl.J.Med.359, 1757-1765.
29. Kärre, K. (2002). NK cells, MHC class I molecules and the missing self. Scand. J. Immunol. 55, 221-228.
30. Khambata-Ford, S., Harbison, C. T., Hart, L. L., Awad, M., Xu, L. A., Horak, C. E., Dakhil, S., Hermann, R. C., Lynch, T. J., and Weber, M. R. (2010). Analysis of potential predictive markers of cetuximab benefit in BMS099, a phase III study of cetuximab and first-line tax-ane/carboplatin in advanced non-small-cell lung cancer. J. Clin. Oncol. 28, 918-927.
31. Leung,W. (2011). Use of NK cell activity in cure by transplant. Br. J. Haematol. 155, 14-29.
32. Leung, W., Handgretinger, R., Iyengar, R., Turner, V., Holladay, M. S., and Hale, G. A. (2007). Inhibitory KIR-HLA receptor-ligand mismatch in autologous haematopoietic stem cell transplantation for solid tumour and lymphoma. Br. J. Cancer 97, 539-542.
33. Leung, W., Iyengar, R., Turner, V., Lang, P., Bader, P., Conn, P., Niethammer, D., and Handgretinger, R. (2004). Determinants of antileukemia effects of allogeneic NK cells. J. Immunol. 172, 644-650.
34. Lode, H. N., Xiang, R., Becker, J. C., Gillies, S. D., and Reisfeld, R. A. (1998a). Immunocytokines: a promising approach to cancer immunotherapy. Pharmacol. Ther. 80, 277-292.
35. Lode, H. N., Xiang, R., Dreier, T., Varki, N. M., Gillies, S. D., and Reisfeld, R. A. (1998b). Natural killer cellmediated eradication of neuroblastoma metastases to bone marrow by targeted interleukin-2 therapy. Blood 91, 1706-1715.
36. Miller, J. S., Soignier, Y., Panoskaltsis-Mortari, A., Mcnearney, S. A., Yun, G. H., Fautsch, S. K., Mckenna, D., Le, C., Defor, T. E., Burns, L. J., Orchard, P. J., Blazar, B. R., Wagner, J. E., Slungaard, A., Weisdorf, D. J., Okazaki, I. J., and Mcglave, P. B. (2005). Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105, 3051-3057.
37. Modak, S., and Cheung, N. K. (2007). Disialoganglioside directed immunotherapy of neuroblastoma. Cancer Invest. 25, 67-77.
38. Moretta, L., Bottino, C., Pende, D., Vitale, M., Mingari, M. C., and Moretta, A. (2005). Human natural killer cells: Molecular mechanisms controlling NK cell activation and tumor cell lysis. Immunol. Lett. 100, 7-13.
39. Moretta, L., and Moretta, A. (2004). Killer immunoglobulin-like receptors. Curr. Opin. Immunol. 16, 626-633.
40. Musolino, A., Naldi, N., Bortesi, B., Pezzuolo, D., Capelletti, M., Missale, G., Laccabue, D., Zerbini, A., Camisa, R., Bisagni, G., Neri, T. M., and Ardizzoni, A. (2008). Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J. Clin. Oncol. 26, 1789-1796.
41. Navid, F., Armstrong, M., and Barfield, R. C. (2009). Immune therapies for neuroblastoma. Cancer Biol. Ther. 8, 874-882.
42. Neal,Z. C.,Imboden,M.,Rakhmilevich, A. L., Kim, K. M., Hank, J. A., Surfus, J., Dixon, J. R., Lode, H. N., Reisfeld, R. A., Gillies, S. D., and Sondel, P. M. (2004a). NXS2 murine neuroblastomas express increased levels of MHC class I antigens upon recurrence following NK-dependent immunotherapy. Cancer Immunol. Immunother. 53, 41-52.
43. Neal, Z. C., Yang, J. C., Rakhmilevich, A. L., Buhtoiarov, I. N., Lum, H. E., Imboden, M., Hank, J. A., Lode, H. N., Reisfeld, R. A., Gillies, S. D., and Sondel,P. M. (2004b). Enhanced activity of hu14.18-IL2 immunocytokine against murine NXS2 neuroblastoma when combined with interleukin 2 therapy. Clin. Cancer Res. 10, 4839-4847.
44. Nimmerjahn, F., and Ravetch, J. V. (2008). Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34-47.
45. O'Byrne, K. J., Gatzemeier, U., Bondarenko, I., Barrios, C., Eschbach, C., Martens, U. M., Hotko, Y., Kortsik, C., Paz-Ares, L., Pereira, J. R., Von Pawel, J., Ramlau, R., Roh, J. K., Yu, C. T., Stroh, C., Celik, I., Schueler, A., and Pirker,R. (2011). Molecular biomarkers in non-small-cell lung cancer: a retrospective analysis of data from the phase 3 FLEX study. Lancet Oncol. 12, 795-805.
46. Oliva, A., Kinter, A. L., Vaccarezza, M., Rubbert, A., Catanzaro, A., Moir, S., Monaco, J., Ehler, L., Mizell, S., Jackson, R., Li, Y., Romano, J. W., and Fauci, A. S. (1998). Natural killer cells from human immunodeficiency virus (HIV)-infected individuals are an important source of CC-chemokines and suppress HIV-1 entry and replication in vitro. J. Clin. Invest. 102, 223-231.
47. Orange, J. S. (2008). Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 8, 713-725.
48. Orange, J. S., Harris, K. E., Andzelm, M. M., Valter, M. M., Geha, R. S., and Strominger, J. L. (2003). The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl. Acad. Sci. U.S.A. 100, 14151-14156.
49. Orr, M. T., Murphy, W. J., and Lanier, L. L. (2010). 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat. Immunol. 11, 321-327.
50. Osenga, K. L., Hank, J. A., Albertini, M. R., Gan, J., Sternberg, A. G., Eickhoff, J., Seeger, R. C., Matthay, K. K., Reynolds, C. P., Twist, C., Krailo, M., Adamson, P. C., Reisfeld, R. A., Gillies, S. D., Sondel, P. M., and Group, C. S. O. (2006). A phase I clinical trial of the hu14.18-IL2 (EMD 273063) as a treatment for children with refractory or recurrent neuroblastoma and melanoma: a study of the Children's Oncology Group. Clin. Cancer Res. 12, 1750-1759.
51. Primus, F. J., Finch, M. D., Wetzel, S. A., Masci, A. M., Schlom, J., and Kashmiri, S. V. (1994). Monoclonal antibody gene transfer. Implications for tumor-specific cellmediated cytotoxicity. Ann. N. Y. Acad. Sci. 716, 154-165; discussion 165-156.
52. Purdy,A. K.,and Campbell,K. S. (2009). Natural killer cells and cancer: regulation by the killer cell Ig-like receptors (KIR). Cancer Biol. Ther. 8, 2211-2220.
53. Ravetch, J. V., and Bolland, S. (2001). IgG Fc receptors. Annu. Rev. Immunol. 19, 275-290.
54. Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W. D., Tosti, A., Posati, S., Rogaia, D., Frassoni, F., Aversa, F., Martelli, M. F., and Velardi, A. (2002). Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295, 2097-2100.
55. Ruggeri, L., Mancusi, A., Capanni, M., Urbani, E., Carotti, A., Aloisi, T., Stern, M., Pende, D., Perruccio, K., Burchielli, E., Topini, F., Bianchi, E., Aversa, F., Martelli, M. F., and Velardi, A. (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.
56. Schrama, D., Reisfeld, R. A., and Becker, J. C. (2006). Antibody targeted drugs as cancer therapeutics. Nat. Rev. Drug Discov. 5, 147-159.
57. Shusterman, S., London, W. B., Gillies, S. D., Hank, J. A., Voss, S. D., Seeger, R. C., Reynolds, C. P., Kimball, J., Albertini, M. R., Wagner, B., Gan, J., Eickhoff, J., Desantes, K. B., Cohn, S. L., Hecht, T., Gadbaw, B., Reisfeld, R. A., Maris, J. M., and Sondel, P. M. (2010). Antitumor activity of hu14.18-IL2 in patients with relapsed/refractory neuroblastoma: a Children's Oncology Group (COG) phase II study. J. Clin. Oncol. 28, 4969-4975.
58. Simon, T., Hero, B., Faldum, A., Handgretinger, R., Schrappe, M., Klingebiel, T., and Berthold, F. (2011). Long term outcome of high-risk neuroblastoma patients after immunotherapy with antibody ch14.18 or oral metronomic chemotherapy. BMC Cancer 11, 21. doi:10.1186/1471-2407-11-21
59. Simon, T., Hero, B., Faldum, A., Handgretinger, R., Schrappe, M., Niethammer, D., and Berthold, F. (2004). Consolidation treatment with chimeric anti-GD2-antibody ch14.18 in children older than 1 year with metastatic neuroblastoma. J. Clin. Oncol. 22, 3549-3557.
60. Sosman, J. A., Hank, J. A., and Sondel, P. M. (1990). In vivo activation of lymphokine-activated killer activity with interleukin-2: prospects for combination therapies. Semin. Oncol. 17, 22-30; discussion 38-41.
61. Taylor, R. J., Chan, S. L., Wood, A., Voskens, C. J., Wolf, J. S., Lin, W., Chapoval, A., Schulze, D. H., Tian, G., and Strome, S. E. (2009). FcgammaRIIIa polymorphisms and cetuximab induced cytotoxicity in squamous cell carcinoma of the head and neck. Cancer Immunol. Immunother. 58, 997-1006.
62. Velardi, A. (2008). Role of KIRs and KIR ligands in hematopoietic transplantation. Curr. Opin. Immunol. 20, 581-587.
63. Venstrom, J. M., Zheng, J., Noor, N., Danis, K. E., Yeh, A. W., Cheung, I. Y., Dupont, B., O'Reilly, R. J., Cheung, N. K., and Hsu, K. C. (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.
64. Vilches, C., and Parham, P. (2002). KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 20, 217-251.
65. Vivier, E., Raulet, D. H., Moretta, A., Caligiuri, M. A., Zitvogel, L., Lanier, L. L., Yokoyama, W. M., and Ugolini, S. (2011). Innate or adaptive immunity? The example of natural killer cells. Science 331, 44-49.
66. Weiner, L. M., Dhodapkar, M. V., and Ferrone, S. (2009). Monoclonal antibodies for cancer immunotherapy. Lancet 373, 1033-1040.
67. Weng, W. K., and Levy, R. (2003). Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J. Clin. Oncol. 21, 3940-3947.
68. Yamane, B. H., Hank, J. A., Albertini, M. R., and Sondel, P. M. (2009). The development of antibody-IL-2 based immunotherapy with hu14.18-IL2 (EMD-273063) in melanoma and neuroblastoma. Expert Opin. Investig. Drugs 18, 991-1000.
69. Yang, R. K., and Sondel, P. M. (2010). Anti-GD2 Strategy in the Treatment of Neuroblastoma. Drugs Future 35, 665.
70. Yu, A. L., Gilman, A. L., Ozkaynak, M. F., London, W. B., Kreissman, S. G., Chen, H. X., Smith, M., Anderson, B., Villablanca, J. G., Matthay, K. K., Shimada, H., Grupp, S. A., Seeger, R., Reynolds, C. P., Buxton, A., Reisfeld, R.A.,Gillies,S. D.,Cohn,S. L.,Maris, J. M., Sondel, P. M., and Group, C. S. O. (2010). Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N.Engl.J.Med.363, 1324-1334.
71. Zhang, W., Gordon, M., Schultheis, A. M., Yang, D. Y., Nagashima, F., Azuma, M., Chang, H. M., Borucka, E., Lurje, G., Sherrod, A. E., Iqbal, S., Groshen, S., and Lenz, H. J. (2007). FCGR2A and FCGR3A polymorphisms associated with clinical outcome of epidermal growth factor receptor expressing metastatic colorectal cancer patients treated with singleagent cetuximab. J. Clin. Oncol. 25, 3712-3718.
72. Zompi, S., and Colucci, F. (2005). Anatomy of a murder-signal transduction pathways leading to activation of natural killer cells. Immunol. Lett. 97, 31-39.