Antibody-cytokine fusion proteins: Innovative weapons in the war against cancer

Clinical and Experimental Medicine

Volumn 4, Issue 2, 2004, Pages 57-64

  Dela Cruz, J S ^a   Huang, T H ^a   Penichet, M L ^a   Morrison, S L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antibody; Antibody fusion protein; Cancer; Cytokine; Immunotherapy

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYBRID PROTEIN; RECOMBINANT INTERLEUKIN 12; RECOMBINANT INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA;

ANTINEOPLASTIC ACTIVITY; CANCER; CELL SURFACE; CLINICAL TRIAL; DRUG DOSE REDUCTION; DRUG EFFICACY; GENE OVEREXPRESSION; HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIDE EFFECT; TREATMENT WITHDRAWAL;

ANTIBODIES; CYTOKINES; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN-12; INTERLEUKIN-2; NEOPLASMS; RECOMBINANT FUSION PROTEINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 8644240039     PISSN: 15918890     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10238-004-0039-y     Document Type: Review

References (83)

1. Arai KI, Lee F, Miyajima A, Miyatake S, Arai N, Yokota T (1990) Cytokines: coordinators of immune and inflammatory responses. Annu Rev Biochem 59:783-836
2. Sule NS, Nerurkar RP, Kamath S (2001) Interleukin-2 as a therapeutic agent. J Assoc Physicians India 49:897-900
3. Rosenberg SA, Lotze MT, Muul LM, Leitman S, Chang AE, Ettinghausen SE, Matory YL, Skibber JM, Shiloni E, Vetto JT et al (1985) Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med 313:1485-1492
4. 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
5. Lotze MT, Chang AE, Seipp CA, Simpson C, Vetto JT, Rosenberg SA (1986) High-dose recombinant interleukin 2 in the treatment of patients with disseminated cancer. Responses, treatment-related morbidity, and histologic findings. JAMA 256:3117-3124
6. Rosenberg SA, Yang JC, White DE, Steinberg SM (1998) Durability of complete responses in patients with metastatic cancer treated with high-dose interleukin-2: identification of the antigens mediating response. Ann Surg 228:307-319
7. Yang JC, Sherry RM, Steinberg SM, Topalian SL, Schwartzentruber DJ, Hwu P, Seipp CA, Rogers-Freezer L, Morton KE, White DE, Liewehr DJ, Merino MJ, Rosenberg SA (2003) Randomized study of high-dose and low-dose interleukin-2 in patients with metastatic renal cancer. J Clin Oncol 21:3127-3132
8. Bruton JK, Koeller JM (1994) Recombinant interleukin-2. Pharmacotherapy 14:635-656
9. Rosenberg SA, Yannelli JR, Yang JC, Topalian SL, Schwartzentruber DJ, Weber JS, Parkinson DR, Seipp CA, Einhorn JH, White DE (1994) Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J Natl Cancer Inst 86:1159-1166
10. Arienti F, Belli F, Rivoltini L, Gambacorti-Passerini C, Furlan L, Mascheroni L, Prada A, Rizzi M, Marchesi E, Vaglini M et al (1993) Adoptive immunotherapy of advanced melanoma patients with interleukin-2 (IL-2) and tumor-infiltrating lymphocytes selected in vitro with low doses of IL-2. Cancer Immunol Immunother 36:315-322
11. Gillies SD, Reilly EB, Lo KM, Reisfeld RA (1992) Antibody-targeted interleukin 2 stimulates T-cell killing of autologous tumor cells. Proc Natl Acad Sci U S A 89:1428-1432
12. Gillies SD, Lo KM, Wesolowski J (1989) High-level expression of chimeric antibodies using adapted cDNA variable region cassettes. J Immunol Methods 125:191-202
13. Sabzevari H, Gillies SD, Mueller BM, Pancook JD, Reisfeld RA (1994) A recombinant antibody-interleukin 2 fusion protein suppresses growth of hepatic human neuroblastoma metastases in severe combined immunodeficiency mice. Proc Natl Acad Sci U S A 91:9626-9630
14. Kendra K, Gan J, Ricci M, Surfus J, Shaker A, Super M, Frost JD, Rakhmilevich A, Hank JA, Gillies SD, Sondel PM (1999) Pharmacokinetics and stability of the ch14.18-interleukin-2 fusion protein in mice. Cancer Immunol Immunother 48:219-229
15. Becker JC, Pancook JD, Gillies SD, Mendelsohn J, Reisfeld RA (1996) Eradication of human hepatic and pulmonary melanoma metastases in SCID mice by antibody-interleukin 2 fusion proteins. Proc Natl Acad Sci U S A 93:2702-2707
16. Hu P, Hornick JL, Glasky MS, Yun A, Milkie MN, Khawli LA, Anderson PM, Epstein AL (1996) A chimeric Lym1/interleukin 2 fusion protein for increasing tumor vascular permeability and enhancing antibody uptake. Cancer Res 56:4998-5004
17. Matsumoto H, Liao S, Arakawa F, Ueno A, Abe H, Awasthi A, Kuroki M (2002) Targeting of interleukin-2 to human MK-1-expressing carcinoma by fusion with a single-chain Fv of anti-MK-1 antibody. Anticancer Res 22:2001-2007
18. Budagian V, Nanni P, Lollini PL, Musiani P, Di Carlo E, Bulanova E, Paus R, Bulfone-Paus S (2002) Enhanced inhibition of tumour growth and metastasis, and induction of antitumour immunity by IL-2-IgG2b fusion protein. Scand J Immunol 55:484-492
19. Carnemolla B, Borsi L, Balza E, Castellani P, Meazza R, Berndt A, Ferrini S, Kosmehl H, Neri D, Zardi L (2002) Enhancement of the antitumor properties of interleukin-2 by its targeted delivery to the tumor blood vessel extracellular matrix. Blood 99:1659-1665
20. Penichet ML, Dela Cruz JS, Shin SU, Morrison SL (2001) A recombinant IgG3-(IL-2) fusion protein for the treatment of human HER2/neu expressing tumors. Hum Antibodies 10:43-49
21. Christ O, Matzku S, Burger C, Zoller M (2001) Interleukin 2-antibody and tumor necrosis factor-antibody fusion proteins induce different antitumor immune responses in vivo. Clin Cancer Res 7:1385-1397
22. Xu X, Clarke P, Szalai G, Shively JE, Williams LE, Shyr Y, Shi E, Primus FJ (2000) Targeting and therapy of carcinoembryonic antigen-expressing tumors in transgenic mice with an antibody-interleukin 2 fusion protein. Cancer Res 60:4475-4484
23. Zhao L, Rai SK, Grosmaire LS, Ledbetter JA, Fell HP (1999) Construction, expression, and characterization of anticarcinoma sFv fused to IL-2 or GM-CSF. J Hematother Stem Cell Res 8:393-399
24. Sogaard M, Ohlsson L, Kristensson K, Rosendahl A, Sjoberg A, Forsberg G, Kalland T, Dohlsten M (1999) Treatment with tumor-reactive Fab-IL-2 and Fab-staphylococcal enterotoxin A fusion proteins leads to sustained T cell activation, and long-term survival of mice with established tumors. Int J Oncol 15:873-882
25. Melani C, Figini M, Nicosia D, Luison E, Ramakrishna V, Casorati G, Parmiani G, Eshhar Z, Canevari S, Colombo MP (1998) Targeting of interleukin 2 to human ovarian carcinoma by fusion with a single-chain Fv of antifolate receptor anti-body. Cancer Res 58:4146-4154
26. Liu SJ, Sher YP, Ting CC, Liao KW, Yu CP, Tao MH (1998) Treatment of B-cell lymphoma with chimeric IgG and single-chain Fv antibody-interleukin-2 fusion proteins. Blood 92:2103-2112
27. Penichet ML, Harvill ET, Morrison SL (1998) An IgG3-IL-2 fusion protein recognizing a murine B cell lymphoma exhibits effective tumor imaging and antitumor activity. J Interferon Cytokine Res 18:597-607
28. Dreier T, Lode HN, Xiang R, Dolman CS, Reisfeld RA, Kang AS (1998) Recombinant immunocytokines targeting the mouse transferrin receptor: construction and biological activities. Bioconjug Chem 9:482-489
29. Shu L, Qi CF, Hand PH, Schlom J, Kashmiri SV (1995) Generation and characterization of a single-gene encoded single-chain immunoglobulin- interleukin-2 fusion protein. Immunotechnology 1:231-241
30. Xiang R, Lode HN, Dolman CS, Dreier T, Varki NM, Qian X, Lo KM, Lan Y, Super M, Gillies SD, Reisfeld RA (1997) Elimination of established murine colon carcinoma metastases by antibody-interleukin 2 fusion protein therapy. Cancer Res 57:4948-4955
31. Hornick JL, Khawli LA, Hu P, Lynch M, Anderson PM, Epstein AL (1997) Chimeric CLL-1 antibody fusion proteins containing granulocyte-macrophage colony-stimulating factor or interleukin-2 with specificity for B-cell malignancies exhibit enhanced effector functions while retaining tumor targeting properties. Blood 89:4437-4447
32. Lode HN, Xiang R, Dreier T, Varki NM, Gillies SD, Reisfeld RA (1998) Natural killer cell-mediated eradication of neuroblastoma metastases to bone marrow by targeted interleukin-2 therapy. Blood 91:1706-1715
33. Nakao M, Hazama M, Mayumi-Aono A, Hinuma S, Fujisawa Y (1994) Immunotherapy of acute and recurrent herpes simplex virus type 2 infection with an adjuvant-free form of recombinant glycoprotein D-interleukin-2 fusion protein. J Infect Dis 169:787-791
34. Chen TT, Tao MH, Levy R (1994) Idiotype-cytokine fusion proteins as cancer vaccines. Relative efficacy of IL-2, IL-4, and granulocyte-macrophage colony-stimulating factor. J Immunol 153:4775-4787
35. Hazama M, Mayumi-Aono A, Asakawa N, Kuroda S, Hinuma S, Fujisawa Y (1993) Adjuvant-independent enhanced immune responses to recombinant heipes simplex virus type 1 glycoprotein D by fusion with biologically active interleukin-2. Vaccine 11:629-636
36. Hazama M, Mayumi-Aono A, Miyazaki T, Hinuma S, Fujisawa Y (1993) Intranasal immunization against herpes simplex virus infection by using a recombinant glycoprotein D fused with immunomodulating proteins, the B subunit of Escherichia coli heat-labile enterotoxin and interleukin-2. Immunology 78:643-649
37. Harvill ET, Fleming JM, Morrison SL (1996) In vivo properties of an IgG3-IL-2 fusion protein. A general strategy for immune potentiation. J Immunol 157:3165-3170
38. Dela Cruz JS, Lau SY, Ramirez EM, Giovanni CD, Forni G, Morrison SL, Penichet ML (2003) Protein vaccination with the HER2/neu extracellular domain plus anti-HER2/neu anti-body-cytokine fusion proteins induces a protective anti-HER2/neu immune response in mice. Vaccine 21:1317-1326
39. Rovero S, Amici A, Carlo ED, Bei R, Nanni P, Quaglino E, Porcedda P, Boggio K, Smorlesi A, Lollini PL, Landuzzi L, Colombo MP, Giovarelli M, Musiani P, Forni G (2000) DNA vaccination against rat her-2/Neu p185 more effectively inhibits carcinogenesis than transplantable carcinomas in transgenic BALB/c mice. J Immunol 165:5133-5142
40. Hayes DF, Yamauchi H, Broadwater G, Cirrincione CT, Rodrigue SP, Berry DA, Younger J, Panasci LE, Millard F, Duggan DB, Norton L, Henderson IC (2001) Circulating HER-2/erbB-2/c-neu (HER-2) extracellular domain as a prognostic factor in patients with metastatic breast cancer: Cancer and Leukemia Group B Study 8662. Clin Cancer Res 7:2703-2711
41. Ruef C, Coleman DE (1990) Granulocyte-macrophage colony-stimulating factor: pleiotropic cytokine with potential clinical usefulness. Rev Infect Dis 12:41-62
42. Batova A, Kamps A, Gillies SD, Reisfeld RA, Yu AL (1999) The Ch14.18-GM-CSF fusion protein is effective at mediating antibody-dependent cellular cytotoxicity and complement-dependent cytotoxicity in vitro. Clin Cancer Res 5:4259-4263
43. Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, Jackson V, Hamada H, Pardoll D, Mulligan RC (1993) Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci U S A 90:3539-3543
44. Tao MH, Levy R (1993) Idiotype/granulocyte-macrophage colony-stimulating factor fusion protein as a vaccine for B-cell lymphoma. Nature 362:755-758
45. Gillies SD, Young D, Lo KM, Roberts S (1993) Biological activity and in vivo clearance of antitumor antibody/cytokine fusion proteins. Bioconjug Chem 4:230-235
46. Dela Cruz JS, Trinh KR, Morrison SE, Penichet ME (2000) Recombinant anti-human HER2/neu IgG3-(GM-CSF) fusion protein retains antigen specificity and cytokine function and demonstrates antitumor activity. J Immunol 165:5112-5121
47. Whittington HA, Ashworth EJ, Hawkins RE (1998) Recombinant adenoviral delivery for in vivo expression of scFv antibody fusion proteins. Gene Ther 5:770-777
48. Burgess AW, Metcalf D (1977) Serum half-life and organ distribution of radiolabeled colony stimulating factor in mice. Exp Hematol 5:456-464
49. Podlaski FJ, Nanduri VB, Hulmes JD, Pan YC, Levin W, Danho W, Chizzonite R, Gately MK, Stern AS (1992) Molecular characterization of interleukin 12. Arch Biochem Biophys 294:230-237
50. Gracie JA, Bradley JA (1996) Interleukin-12 induces interferon-gamma- dependent switching of IgG alloantibody subclass. Eur J Immunol 26:1217-1221
51. Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM (1993) Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 260:547-549
52. Farrar MA, Schreiber RD (1993) The molecular cell biology of interferon-gamma and its receptor. Annu Rev Immunol 11:571-611
53. Gately MK, Warrier RR, Honasoge S, Carvajal DM, Faherty DA, Connaughton SE, Anderson TD, Sarmiento U, Hubbard BR, Murphy M (1994) Administration of recombinant IL-12 to normal mice enhances cytolytic lymphocyte activity and induces production of IFN-gamma in vivo. Int Immunol 6:157-167
54. Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, Loudon R, Sherman F, Perussia B, Trinchieri G (1989) Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 170:827-845
55. Chan SH, Perussia B, Gupta JW, Kobayashi M, Pospisil M, Young HA, Wolf SF, Young D, Clark SC, Trinchieri G (1991) Induction of interferon gamma production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other inducers. J Exp Med 173:869-879
56. Voest EE, Kenyon BM, O'Reilly MS. Truitt G, D'Amato RJ, Folkman J (1995) Inhibition of angiogenesis in vivo by interleukin 12. J Natl Cancer Inst 87:581-586
57. Brunda MJ, Luistro L, Warrier RR, Wright RB, Hubbard BR, Murphy M, Wolf SF, Gately MK (1993) Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J Exp Med 178:1223-1230
58. Nastala CL, Edington HD, McKinney TG, Tahara H, Nalesnik MA, Brunda MJ, Gately MK, Wolf SF, Schreiber RD, Storkus WJ et al (1994) Recombinant IL-12 administration induces tumor regression in association with IFN-gamma production. J Immunol 153:1697-1706
59. Soiffer RJ, Robertson MJ, Murray C, Cochran K, Ritz J (1993) Interleukin-12 augments cytolytic activity of peripheral blood lymphocytes from patients with hematologic and solid malignancies. Blood 82:2790-2796
60. Andrews EJ (1972) An in vivo evaluation of the immunosuppressive action of bleomycin. Cancer Res 32:1993-1994
61. Zeh HJ 3rd, Hurd S, Storkus WJ, Lotze MT (1993) Interleukin-12 promotes the proliferation and cytolytic maturation of immune effectors: implications for the immunotherapy of cancer. J Immunother 14:155-161
62. Atkins MB, Robertson MJ, Gordon M, Lotze MT, DeCoste M, DuBois JS, Ritz I, Sandler AB, Edington HD, Garzone PD, Mier JW, Canning CM, Battiato L, Tahara H, Sherman ML (1997) Phase I evaluation of intravenous recombinant human interleukin 12 in patients with advanced malignancies. Clin Cancer Res 3:409-417
63. Gollob JA, Veenstra KG, Mier JW, Atkins MB (2001) Agranulocytosis and hemolytic anemia in patients with renal cell cancer treated with interleukin-12. J Immunother 24:91-98
64. Gillies SD, Lan Y, Wesolowski JS, Qian X, Reisfeld RA, Holden S, Super M, Lo KM (1998) Antibody-IL-12 fusion proteins are effective in SCID mouse models of prostate and colon carcinoma metastases. J Immunol 160:6195-6203
65. Peng LS, Penichet ML, Morrison SL (1999) A single-chain IL-12 IgG3 antibody fusion protein retains antibody specificity and IL-12 bioactivity and demonstrates antitumor activity. J Immunol 163:250-258
66. Lieschke GJ, Rao PK, Gately MK, Mulligan RC (1997) Bioactive murine and human interleukin-12 fusion proteins which retain antitumor activity in vivo. Nat Biotechnol 15:35-40
67. Peng LS, Penichet ML, Dela Cruz JS, Sampogna SL, Morrison SL (2001) Mechanism of antitumor activity of a single-chain interleukin-12 IgG3 antibody fusion protein (mscIL-12.her2.IgG3). J Interferon Cytokine Res 21:709-720
68. Chan SH, Kobayashi M, Santoli D, Perussia B, Trinchieri G (1992) Mechanisms of IFN-gamma induction by natural killer cell stimulatory factor (NKSF/IL-12). Role of transcription and mRNA stability in the synergistic interaction between NKSF and IL-2. J Immunol 148:92-98
69. Jong R de, Janson AA, Faber WR, Naafs B, Ottenhoff TH (1997) IL-2 and IL-12 act in synergy to overcome antigenspecific T cell unresponsiveness in mycobacterial disease. J Immunol 159:786-793
70. Wigginton JM, Park JW, Gruys ME, Young HA, Jorcyk CL, Back TC, Brunda MJ, Strieter RM, Ward J, Green JE, Wiltrout RH (2001) Complete regression of established spontaneous mammary carcinoma and the therapeutic prevention of genetically programmed neoplastic transition by IL-12/pulse IL-2: induction of local T cell infiltration, Fas/Fas ligand gene expression, and mammary epithelial apoptosis. J Immunol 166:1156-1168
71. Gillies SD, Lan Y, Brunkhorst B, Wong WK, Li Y, Lo KM (2002) Bi-functional cytokine fusion proteins for gene therapy and antibody-targeted treatment of cancer. Cancer Immunol Immunother 51:449-460
72. Aggarwal BB, Kohr WJ, Hass PE, Moffat B, Spencer SA, Henzel WJ, Bringman TS, Nedwin GE, Goeddel DV, Harkins RN (1985) Human tumor necrosis factor. Production, purification, and characterization. J Biol Chem 260:2345-2354
73. Laster SM, Wood JG, Gooding LR (1988) Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J Immunol 141:2629-2634
74. Nawroth P, Handley D, Matsueda G, De Waal R, Gerlach H, Blohm D, Stem D (1988) Tumor necrosis factor/cachectin-induced intravascular fibrin formation in meth A fibrosarcomas. J Exp Med 168:637-647
75. Candido KA, Shimizu K, McLaughlin JC, Kunkel R, Fuller JA, Redman BG, Thomas EK, Nickoloff BJ, Mule JJ (2001) Local administration of dendritic cells inhibits established breast tumor growth: implications for apoptosis-inducing agents. Cancer Res 61:228-236
76. Asher A, Mule JJ, Reichert CM, Shiloni E, Rosenberg SA (1987) Studies on the anti-tumor efficacy of systemically administered recombinant tumor necrosis factor against several murine tumors in vivo. J Immunol 138:963-974
77. Robert B, Mach JP, Mani JC, Ychou M, Folli S, Artus JC, Pelegrin A (1996) Cytokine targeting in tumors using a bispecific antibody directed against carcinoembryonic antigen and tumor necrosis factor alpha. Cancer Res 56:4758-4765
78. Moro M, Pelagi M, Fulci G, Paganelli G, Dellabona P, Casorati G, Siccardi AG, Corti A (1997) Tumor cell targeting with antibody-avidin complexes and biotinylated tumor necrosis factor alpha. Cancer Res 57:1922-1928
79. Cooke SP, Pedley RB, Boden R, Begent RH, Chester KA (2002) In vivo tumor delivery of a recombinant single chain Fv::tumor necrosis factor-alpha fusion [correction of factor: a fusion] protein. Bioconjug Chem 13:7-15
80. Borsi L, Balza E, Camemolla B, Sassi F, Castellani P, Berndt A, Kosmehl H, Biro A, Siri A, Orecchia P, Grassi J, Neri D, Zardi L (2003) Selective targeted delivery of TNF{alpha} to tumor blood vessels. Blood 102:4384-4392
81. Halin C, Gafner V, Villani ME, Borsi L, Berndt A, Kosmehl H, Zardi L, Neri D (2003) Synergistic therapeutic effects of a tumor targeting antibody fragment, fused to interleukin 12 and to tumor necrosis factor alpha. Cancer Res 63:3202-3210
82. Maroof A (2001) Generation of murine bone-marrow-derived dendritic cell. In: Robinson SP, Stagg AJ (eds) Dendritic cell protocols. Human Press, Totowa, New Jersey, pp 191-198
83. Hank JA, Albertini M, Gan J, Surfus J, Sternberg A, King D, Schalch H, Kim K, Eickhoff J, Reisfeld RA, Gillies S, Sondel PM (2003) Clinical administration of antibody-cytokine hu14.18-IL-2 induces IL-2-mediated immune activation. American Association for Cancer Research. 94th Annual Meeting Proceedings, July 2003. Vol 44, 2nd edn