Synergistic innate and adaptive immune response to combination immunotherapy with anti-tumor antigen antibodies and extended serum half-life il-2

Cancer Cell

Volumn 27, Issue 4, 2015, Pages 489-501

  Zhu, Eric F ^a,b   Gai, Shuning A ^a,b   Opel, Cary F ^a,b   Kwan, Byron H ^a,b   Surana, Rishi ^c   Mihm, Martin C ^d,e   Kauke, Monique J ^a,b   Moynihan, Kelly D ^a,b   Angelini, Alessandro ^b   Williams, Robert T ^b   Stephan, Matthias T ^a,b   Kim, Jacob S ^b   Yaffe, Michael B ^a,b   Irvine, Darrell J ^a,b,f   Weiner, Louis M ^c   Dranoff, Glenn ^d   Wittrup, K Dane ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c GEORGETOWN UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDESLEUKIN; CD8 ANTIGEN; CXCL3 CHEMOKINE; CYTOKINE; MONCOLONAL ANTIBODY TA99; MONOCLONAL ANTIBODY; TUMOR ANTIGEN; UNCLASSIFIED DRUG; INTERLEUKIN 2;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; CANCER CONTROL; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CYTOKINE STORM; DRUG EFFICACY; DRUG POTENCY; EFFECTOR CELL; HALF LIFE TIME; IMMUNOLOGICAL MEMORY; INNATE IMMUNITY; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MELANOMA; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; TUMOR MODEL; ANIMAL; C57BL MOUSE; DRUG EFFECTS; DRUG POTENTIATION; IMMUNOLOGY; IMMUNOTHERAPY; METABOLISM; NEOPLASMS;

ADAPTIVE IMMUNITY; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DRUG SYNERGISM; HALF-LIFE; IMMUNITY, INNATE; IMMUNOTHERAPY; INTERLEUKIN-2; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; NEOPLASMS;

EID: 84928013457     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.03.004     Document Type: Article

References (71)

1. Abès R., Gélizé E., Fridman W.H., Teillaud J.-L. Long-lasting antitumor protection by anti-CD20 antibody through cellular immune response. Blood 2010, 116:926-934.
2. Allavena P., Sica A., Vecchi A., Locati M., Sozzani S., Mantovani A. The chemokine receptor switch paradigm and dendritic cell migration: its significance in tumor tissues. Immunol. Rev. 2000, 177:141-149.
3. Anderson C.L., Chaudhury C., Kim J., Bronson C.L., Wani M.A., Mohanty S. Perspective- FcRn transports albumin: relevance to immunology and medicine. Trends Immunol. 2006, 27:343-348.
4. Bajorin D.F., Chapman P.B., Wong G., Coit D.G., Kunicka J., Dimaggio J., Cordon-Cardo C., Urmacher C., Dantes L., Templeton M.A., et al. Phase I evaluation of a combination of monoclonal antibody R24 and interleukin 2 in patients with metastatic melanoma. Cancer Res. 1990, 50:7490-7495.
5. Baley P.A., Yoshida K., Qian W., Sehgal I., Thompson T.C. Progression to androgen insensitivity in a novel invitro mouse model for prostate cancer. J.Steroid Biochem. Mol. Biol. 1995, 52:403-413.
6. Balkwill F., Charles K.A., Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005, 7:211-217.
7. Baudino L., Shinohara Y., Nimmerjahn F., Furukawa J., Nakata M., Martínez-Soria E., Petry F., Ravetch J.V., Nishimura S., Izui S. Crucial role of aspartic acid at position 265 in the CH2 domain for murine IgG2a and IgG2b Fc-associated effector functions. J.Immunol. 2008, 181:6664-6669.
8. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., Koup R.A. Sensitive and viable identification of antigen-specific CD8+ Tcells by a flow cytometric assay for degranulation. J.Immunol. Methods 2003, 281:65-78.
9. Bleumer I., Oosterwijk E., Oosterwijk-Wakka J.C., Völler M.C., Melchior S., Warnaar S.O., Mala C., Beck J., Mulders P.F.A. A clinical trial with chimeric monoclonal antibody WX-G250 and low dose interleukin-2 pulsing scheme for advanced renal cell carcinoma. J.Urol. 2006, 175:57-62.
10. Buonocore S., Haddou N.O., Moore F., Florquin S., Paulart F., Heirman C., Thielemans K., Goldman M., Flamand V. Neutrophil-dependent tumor rejection and priming of tumoricidal CD8+ Tcell response induced by dendritic cells overexpressing CD95L. J.Leukoc. Biol. 2008, 84:713-720.
11. Carson W.E., Parihar R., Lindemann M.J., Personeni N., Dierksheide J., Meropol N.J., Baselga J., Caligiuri M.A. Interleukin-2 enhances the natural killer cell response to Herceptin-coated Her2/neu-positive breast cancer cells. Eur. J. Immunol. 2001, 31:3016-3025.
12. Cassatella M.A. The production of cytokines by polymorphonuclear neutrophils. Immunol. Today 1995, 16:21-26.
13. Clemente C.G., Mihm M.C., Bufalino R., Zurrida S., Collini P., Cascinelli N. Prognostic value of tumor infiltrating lymphocytes inthe vertical growth phase of primary cutaneous melanoma. Cancer 1996, 77:1303-1310.
14. Clynes R.A., Towers T.L., Presta L.G., Ravetch J.V. Inhibitory Fc receptors modulate invivo cytotoxicity against tumor targets. Nat. Med. 2000, 6:443-446.
15. Colotta F., Re F., Polentarutti N., Sozzani S., Mantovani A. Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 1992, 80:2012-2020.
16. Dyall R., Vasovic L.V., Clynes R.A., Nikolić-Zugić J. Cellular requirements for the monoclonal antibody-mediated eradication of an established solid tumor. Eur. J. Immunol. 1999, 29:30-37.
17. Eisenbeis C.F., Caligiuri M.A., Byrd J.C. Rituximab: converging mechanisms of action in non-Hodgkin's lymphoma?. Clin. Cancer Res. 2003, 9:5810-5812.
18. Eisenbeis C.F., Grainger A., Fischer B., Baiocchi R.A., Carrodeguas L., Roychowdhury S., Chen L., Banks A.L., Davis T., Young D., et al. Combination immunotherapy of B-cell non-Hodgkin's lymphoma with rituximab and interleukin-2: a preclinical and phase I study. Clin. Cancer Res. 2004, 10:6101-6110.
19. Fang F.C. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2004, 2:820-832.
20. Feau S., Arens R., Togher S., Schoenberger S.P. Autocrine IL-2 is required for secondary population expansion of CD8(+) memory Tcells. Nat. Immunol. 2011, 12:908-913.
21. Ferris R.L., Jaffee E.M., Ferrone S. Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J.Clin. Oncol. 2010, 28:4390-4399.
22. Fleming G.F., Meropol N.J., Rosner G.L., Hollis D.R., Carson W.E., Caligiuri M., Mortimer J., Tkaczuk K., Parihar R., Schilsky R.L., Ratain M.J. A phase I trial of escalating doses of trastuzumab combined with daily subcutaneous interleukin 2: report of cancer and leukemia group B 9661. Clin. Cancer Res. 2002, 8:3718-3727.
23. Fridlender Z.G., Albelda S.M. Tumor-associated neutrophils: friend or foe?. Carcinogenesis 2012, 33:949-955.
24. Gabrilovich D.I., Ostrand-Rosenberg S., Bronte V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012, 12:253-268.
25. Gross S., Gammon S.T., Moss B.L., Rauch D., Harding J., Heinecke J.W., Ratner L., Piwnica-Worms D. Bioluminescence imaging of myeloperoxidase activity invivo. Nat. Med. 2009, 15:455-461.
26. Guo R.-F., Ward P.A. Role of C5a in inflammatory responses. Annu. Rev. Immunol. 2005, 23:821-852.
27. Huizinga T.W.J., van der Schoot C.E., Jost C., Klaassen R., Kleijer M., von dem Borne A.E.G.K., Roos D., Tetteroo P.A.T. The PI-linked receptor FcRIII is released on stimulation of neutrophils. Nature 1988, 333:667-669.
28. Huntington N.D., Tabarias H., Fairfax K., Brady J., Hayakawa Y., Degli-Esposti M.A., Smyth M.J., Tarlinton D.M., Nutt S.L. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J.Immunol. 2007, 178:4764-4770.
29. Jackson S.H., Gallin J.I., Holland S.M. The p47phox mouse knock-out model of chronic granulomatous disease. J.Exp. Med. 1995, 182:751-758.
30. Jones S.A. Directing transition from innate to acquired immunity: defining a role for IL-6. J.Immunol. 2005, 175:3463-3468.
31. Ju S.-A., Lee S.-C., Kwon T.-H., Heo S.-K., Park S.-M., Paek H.-N., Suh J.-H., Cho H.R., Kwon B., Kwon B.S., Kim B.S. Immunity to melanoma mediated by 4-1BB is associated with enhanced activity of tumour-infiltrating lymphocytes. Immunol. Cell Biol. 2005, 83:344-351.
32. June C.H. Principles of adoptive Tcell cancer therapy. J.Clin. Invest. 2007, 117:1204-1212.
33. Kalia V., Sarkar S., Subramaniam S., Haining W.N., Smith K.A., Ahmed R. Prolonged interleukin-2Ralpha expression on virus-specific CD8+ Tcells favors terminal-effector differentiation invivo. Immunity 2010, 32:91-103.
34. Keir M.E., Butte M.J., Freeman G.J., Sharpe A.H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 2008, 26:677-704.
35. Khan K.D., Emmanouilides C., Benson D.M., Hurst D., Garcia P., Michelson G., Milan S., Ferketich A.K., Piro L., Leonard J.P., et al. A phase 2 study of rituximab in combination with recombinant interleukin-2 for rituximab-refractory indolent non-Hodgkin's lymphoma. Clin. Cancer Res. 2006, 12:7046-7053.
36. Konrad M.W., Hemstreet G., Hersh E.M., Mansell P.W.A., Mertelsmann R., Kolitz J.E., Bradley E.C. Pharmacokinetics of recombinant interleukin 2 in humans. Cancer Res. 1990, 50:2009-2017.
37. Kuijpers T.W., Tool A.T., van der Schoot C.E., Ginsel L.A., Onderwater J.J., Roos D., Verhoeven A.J. Membrane surface antigen expression on neutrophils: a reappraisal of the use of surface markers for neutrophil activation. Blood 1991, 78:1105-1111.
38. Lacy P., Stow J.L. Cytokine release from innate immune cells: association with diverse membrane trafficking pathways. Blood 2011, 118:9-18.
39. Liao W., Lin J.-X., Leonard W.J. Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity 2013, 38:13-25.
40. Lillard J.W., Boyaka P.N., Chertov O., Oppenheim J.J., McGhee J.R. Mechanisms for induction of acquired host immunity by neutrophil peptide defensins. Proc. Natl. Acad. Sci. USA 1999, 96:651-656.
41. Mani A., Roda J., Young D., Caligiuri M.A., Fleming G.F., Kaufman P., Brufsky A., Ottman S., Carson W.E., Shapiro C.L. A phase II trial of trastuzumab in combination with low-dose interleukin-2 (IL-2) in patients (PTS) with metastatic breast cancer (MBC) who have previously failed trastuzumab. Breast Cancer Res. Treat. 2009, 117:83-89.
42. Müller I., Munder M., Kropf P., Hänsch G.M. Polymorphonuclear neutrophils and T lymphocytes: strange bedfellows or brothers in arms?. Trends Immunol. 2009, 30:522-530.
43. Neckers L.M., Cossman J. Transferrin receptor induction in mitogen-stimulated human T lymphocytes is required for DNA synthesis and cell division and is regulated by interleukin 2. Proc. Natl. Acad. Sci. USA 1983, 80:3494-3498.
44. Overwijk W.W. Breaking tolerance in cancer immunotherapy: time to ACT. Curr. Opin. Immunol. 2005, 17:187-194.
45. Park S., Jiang Z., Mortenson E.D., Deng L., Radkevich-Brown O., Yang X., Sattar H., Wang Y., Brown N.K., Greene M., et al. The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell 2010, 18:160-170.
46. Pelletier M., Micheletti A., Cassatella M.A. Modulation of human neutrophil survival and antigen expression by activated CD4+ and CD8+ Tcells. J.Leukoc. Biol. 2010, 88:1163-1170.
47. Pipkin M.E., Sacks J.A., Cruz-Guilloty F., Lichtenheld M.G., Bevan M.J., Rao A. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic Tcells. Immunity 2010, 32:79-90.
48. Poiré X., Kline J., Grinblatt D., Zimmerman T., Conner K., Muhs C., Gajewski T., Van Besien K., Smith S.M. Phase II study of immunomodulation with granulocyte-macrophage colony-stimulating factor, interleukin-2, and rituximab following autologous stem cell transplant in patients with relapsed or refractory lymphomas. Leuk. Lymphoma 2010, 51:1241-1250.
49. Pollard J.W. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 2004, 4:71-78.
50. Rao B.M., Driver I., Lauffenburger D.A., Wittrup K.D. High-affinity CD25-binding IL-2 mutants potently stimulate persistent Tcell growth. Biochemistry 2005, 44:10696-10701.
51. Repka T., Chiorean E.G., Gay J., Herwig K.E., Kohl V.K., Yee D., Miller J.S. Trastuzumab and interleukin-2 in HER2-positive metastatic breast cancer: a pilot study. Clin. Cancer Res. 2003, 9:2440-2446.
52. Schneider-Merck T., Lammerts van Bueren J.J., Berger S., Rossen K., van Berkel P.H.C., Derer S., Beyer T., Lohse S., Bleeker W.K., Peipp M., et al. Human IgG2 antibodies against epidermal growth factor receptor effectively trigger antibody-dependent cellular cytotoxicity but, in contrast to IgG1, only by cells of myeloid lineage. J.Immunology 2010, 184:512-520.
53. Schwartz R.H. T cell anergy. Annu. Rev. Immunol. 2003, 21:305-334.
54. Siders W.M., Shields J., Garron C., Hu Y., Boutin P., Shankara S., Weber W., Roberts B., Kaplan J.M. Involvement of neutrophils and natural killer cells in the anti-tumor activity of alemtuzumab in xenograft tumor models. Leuk. Lymphoma 2010, 51:1293-1304.
55. Sliwkowski M.X., Lofgren J.A., Lewis G.D., Hotaling T.E., Fendly B.M., Fox J.A. Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin). Semin. Oncol. 1999, 26(4, Suppl 12):60-70.
56. Stagg J., Johnstone R.W., Smyth M.J. From cancer immunosurveillance to cancer immunotherapy. Immunol. Rev. 2007, 220:82-101.
57. Stagg J., Loi S., Divisekera U., Ngiow S.F., Duret H., Yagita H., Teng M.W., Smyth M.J. Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc. Natl. Acad. Sci. USA 2011, 108:7142-7147.
58. Suntharalingam G., Perry M.R., Ward S., Brett S.J., Castello-Cortes A., Brunner M.D., Panoskaltsis N. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N.Engl. J. Med. 2006, 355:1018-1028.
59. van Elsas A., Hurwitz A.A., Allison J.P. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J.Exp. Med. 1999, 190:355-366.
60. Vasović L.V., Dyall R., Clynes R.A., Ravetch J.V., Nikolić-Zugic J. Synergy between an antibody and CD8+ cells in eliminating an established tumor. Eur. J. Immunol. 1997, 27:374-382.
61. Walunas T.L., Lenschow D.J., Bakker C.Y., Linsley P.S., Freeman G.J., Green J.M., Thompson C.B., Bluestone J.A. CTLA-4 can function as a negative regulator of Tcell activation. Immunity 1994, 1:405-413.
62. Wang S., Astsaturov I.A., Bingham C.A., McCarthy K.M., von Mehren M., Xu W., Alpaugh R.K., Tang Y., Littlefield B.A., Hawkins L.D., et al. Effective antibody therapy induces host-protective antitumor immunity that is augmented by TLR4 agonist treatment. Cancer Immunol. Immunother. 2012, 61:49-61.
63. Ward P.L., Koeppen H., Hurteau T., Schreiber H. Tumor antigens defined by cloned immunological probes are highly polymorphic and are not detected on autologous normal cells. J.Exp. Med. 1989, 170:217-232.
64. Waugh D.J.J., Wilson C. The interleukin-8 pathway in cancer. Clin. Cancer Res. 2008, 14:6735-6741.
65. Weiner L.M., Dhodapkar M.V., Ferrone S. Monoclonal antibodies for cancer immunotherapy. Lancet 2009, 373:1033-1040.
66. Weng W.-K., Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J.Clin. Oncol. 2003, 21:3940-3947.
67. Winkler U., Jensen M., Manzke O., Schulz H., Diehl V., Engert A. Cytokine-release syndrome in patients with B-cell chronic lymphocytic leukemia and high lymphocyte counts after treatment with an anti-CD20 monoclonal antibody (rituximab, IDEC-C2B8). Blood 1999, 94:2217-2224.
68. Wolpe S.D., Sherry B., Juers D., Davatelis G., Yurt R.W., Cerami A. Identification and characterization of macrophage inflammatory protein 2. Proc. Natl. Acad. Sci. USA 1989, 86:612-616.
69. Yang J.C., Topalian S.L., Schwartzentruber D.J., Parkinson D.R., Marincola F.M., Weber J.S., Seipp C.A., White D.E., Rosenberg S.A. The use of polyethylene glycol-modified interleukin-2 (PEG-IL-2) in the treatment of patients with metastatic renal cell carcinoma and melanoma. A phase I study and a randomized prospective study comparing IL-2 alone versus IL-2 combined with PEG-IL-2. Cancer 1995, 76:687-694.
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., et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N.Engl. J. Med. 2010, 363:1324-1334. Children's Oncology Group.
71. Zhang H., Zhang S., Cheung N.-K.V., Ragupathi G., Livingston P.O. Antibodies against GD2 ganglioside can eradicate syngeneic cancer micrometastases. Cancer Res. 1998, 58:2844-2849.