Role of chitosan co-formulation in enhancing interleukin-12 delivery and antitumor activity

Biomaterials

Volumn 34, Issue 15, 2013, Pages 3828-3836

  Yang, Lirong ^a   Zaharoff, David A ^a  

^a University of Arkansas   (United States)

Author keywords

Chitosan; Immunotherapy; Interleukin 12; Intratumoral; Paracrine delivery

Indexed keywords

ANTI-TUMOR ACTIVITIES; CHITOSAN SOLUTION; CYTOKINE DELIVERY; IMMUNOTHERAPY; INTERLEUKIN-12; INTRATUMORAL; PARACRINE; TUMOR MICROENVIRONMENT;

CELL CULTURE; CELL PROLIFERATION; CHITOSAN; MAMMALS;

TUMORS;

CHITOSAN; GAMMA INTERFERON; INTERLEUKIN 12;

ADENOCARCINOMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; C57BL 6 MOUSE; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG ACTIVITY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; IMMUNOPHENOTYPING; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMISTRY, PHARMACEUTICAL; CHITOSAN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DELIVERY SYSTEMS; FEMALE; HUMANS; INJECTIONS; INTERLEUKIN-12; LEUKOCYTES; MICE; MICE, INBRED C57BL; PHENOTYPE;

MUS;

EID: 84874972738     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.02.031     Document Type: Article

References (48)

1. Bennett I.L., Beeson P.B. Studies on the pathogenesis of fever. II. Characterization of fever-producing substances from polymorphonuclear leukocytes and from the fluid of sterile exudates. J Exp Med 1953, 98:493-508.
2. Golomb H.M., Ratain M.J., Fefer A., Thompson J., Golde D.W., Ozer H., et al. Randomized study of the duration of treatment with interferon alfa-2B in patients with hairy cell leukemia. J Natl Cancer Inst 1988, 80:369-373.
3. Groopman J.E., Gottlieb M.S., Goodman J., Mitsuyasu R.T., Conant M.A., Prince H., et al. Recombinant alpha-2 interferon therapy for Kaposi's sarcoma associated with the acquired immunodeficiency syndrome. Ann Intern Med 1984, 100:671-676.
4. Real F.X., Oettgen H.F., Krown S.E. Kaposi's sarcoma and the acquired immunodeficiency syndrome: treatment with high and low doses of recombinant leukocyte A interferon. J Clin Oncol 1986, 4:544-551.
5. Kantarjian H.M., Smith T.L., O'Brien S., Beran M., Pierce S., Talpaz M. Prolonged survival in chronic myelogenous leukemia after cytogenetic response to interferon-alpha therapy. The leukemia service. Ann Intern Med 1995, 122:254-261.
6. Ozer H., George S.L., Schiffer C.A., Rao K., Rao P.N., Wurster-Hill D.H., et al. Prolonged subcutaneous administration of recombinant alpha 2b interferon in patients with previously untreated Philadelphia chromosome-positive chronic-phase chronic myelogenous leukemia: effect on remission duration and survival: cancer and leukemia group B study 8583. Blood 1993, 82:2975-2984.
7. Rosenberg S.A., Lotze M.T., Muul L.M., Chang A.E., Avis F.P., Leitman S., et al. A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone. N Engl J Med 1987, 316:889-897.
8. Rosenberg S.A., Yang J.C., Topalian S.L., Schwartzentruber D.J., Weber J.S., Parkinson D.R., et al. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin 2. J Am Med Assoc 1994, 271:907-913.
9. Fyfe G., Fisher R.I., Rosenberg S.A., Sznol M., Parkinson D.R., Louie A.C. Results of treatment of 255 patients with metastatic renal cell carcinoma who received high-dose recombinant interleukin-2 therapy. J Clin Oncol 1995, 13:688-696.
10. Atkins M.B., Kunkel L., Sznol M., Rosenberg S.A. High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-term survival update. Cancer J Sci Am 2000, 6(Suppl. 1):S11-S14.
11. Atkins M.B., Lotze M.T., Dutcher J.P., Fisher R.I., Weiss G., Margolin K., et al. High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 1999, 17:2105-2116.
12. Brunda M.J., Luistro L., Rumennik L., Wright R.B., Wigginton J.M., Wiltrout R.H., et al. Interleukin-12: murine models of a potent antitumor agent. Ann N Y Acad Sci 1996, 795:266-274.
13. Hill H.C., Conway T.F., Sabel M.S., Jong Y.S., Mathiowitz E., Bankert R.B., et al. Cancer immunotherapy with interleukin 12 and granulocyte-macrophage colony-stimulating factor-encapsulated microspheres: coinduction of innate and adaptive antitumor immunity and cure of disseminated disease. Cancer Res 2002, 62:7254-7263.
14. Egilmez N.K., Kilinc M.O., Gu T., Conway T.F. Controlled-release particulate cytokine adjuvants for cancer therapy. Endocr Metab Immune Disord Drug Targets 2007, 7:266-270.
15. Arai K., Kinumaki T., Fujita T. Toxicity of chitosan. Bull Tokai Reg Fish Lab 1968, 43:89-94.
16. Singla A.K., Chawla M. Chitosan: some pharmaceutical and biological aspects - an update. J Pharm Pharmacol 2001, 53:1047-1067.
17. McNeela E.A., Jabbal-Gill I., Illum L., Pizza M., Rappuoli R., Podda A., et al. Intranasal immunization with genetically detoxified diphtheria toxin induces T cell responses in humans: enhancement of Th2 responses and toxin-neutralizing antibodies by formulation with chitosan. Vaccine 2004, 22:909-914.
18. Wedmore I., McManus J.G., Pusateri A.E., Holcomb J.B. A special report on the chitosan-based hemostatic dressing: experience in current combat operations. J Trauma 2006, 60:655-658.
19. Zaharoff D.A., Rogers C.J., Hance K.W., Schlom J., Greiner J.W. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine 2007, 25:2085-2094.
20. Zaharoff D.A., Rogers C.J., Hance K.W., Schlom J., Greiner J.W. Chitosan solution enhances the immunoadjuvant properties of GM-CSF. Vaccine 2007, 25:8673-8686.
21. Zaharoff D.A., Hoffman B.S., Hooper H.B., Benjamin C.J., Khurana K.K., Hance K.W., et al. Intravesical immunotherapy of superficial bladder cancer with chitosan/interleukin-12. Cancer Res 2009, 69:6192-6199.
22. Zaharoff D.A., Hance K.W., Rogers C.J., Schlom J., Greiner J.W. Intratumoral immunotherapy of established solid tumors with chitosan/IL-12. J Immunother 2010, 33:697-705.
23. Zhu S., Lee D.A., Li S. IL-12 and IL-27 sequential gene therapy via intramuscular electroporation delivery for eliminating distal aggressive tumors. J Immunol 2010, 184:2348-2354.
24. Cavallo F., Signorelli P., Giovarelli M., Musiani P., Modesti A., Brunda M.J., et al. Antitumor efficacy of adenocarcinoma cells engineered to produce interleukin 12 (IL-12) or other cytokines compared with exogenous IL-12. J Natl Cancer Inst 1997, 89:1049-1058.
25. Zitvogel L., Tahara H., Robbins P.D., Storkus W.J., Clarke M.R., Nalesnik M.A., et al. Cancer immunotherapy of established tumors with IL-12. Effective delivery by genetically engineered fibroblasts. J Immunol 1995, 155:1393-1403.
26. Egilmez N.K., Jong Y.S., Sabel M.S., Jacob J.S., Mathiowitz E., Bankert R.B. In situ tumor vaccination with interleukin-12-encapsulated biodegradable microspheres: induction of tumor regression and potent antitumor immunity. Cancer Res 2000, 60:3832-3837.
27. Watkins S.K., Egilmez N.K., Suttles J., Stout R.D. IL-12 rapidly alters the functional profile of tumor-associated and tumor-infiltrating macrophages in vitro and in vivo. J Immunol 2007, 178:1357-1362.
28. Wesa A., Kalinski P., Kirkwood J.M., Tatsumi T., Storkus W.J. Polarized type-1 dendritic cells (DC1) producing high levels of IL-12 family members rescue patient TH1-type antimelanoma CD4+ T cell responses in vitro. J Immunother 2007, 30:75-82.
29. Egilmez N.K., Kilinc M.O. Tumor-resident CD8+ T-cell: the critical catalyst in IL-12-mediated reversal of tumor immune suppression. Arch Immunol Ther Exp (Warsz) 2010, 58:399-405.
30. Kilinc M.O., Aulakh K.S., Nair R.E., Jones S.A., Alard P., Kosiewicz M.M., et al. Reversing tumor immune suppression with intratumoral IL-12: activation of tumor-associated T effector/memory cells, induction of T suppressor apoptosis, and infiltration of CD8+ T effectors. J Immunol 2006, 177:6962-6973.
31. Kilinc M.O., Rowswell-Turner R.B., Gu T., Virtuoso L.P., Egilmez N.K. Activated CD8+ T-effector/memory cells eliminate CD4+ CD25+ Foxp3+ T-suppressor cells from tumors via FasL mediated apoptosis. J Immunol 2009, 183:7656-7660.
32. Kilinc M.O., Gu T., Harden J.L., Virtuoso L.P., Egilmez N.K. Central role of tumor-associated CD8+ T effector/memory cells in restoring systemic antitumor immunity. J Immunol 2009, 182:4217-4225.
33. Gajewski T.F. Cancer immunotherapy. Mol Oncol 2012, 6:242-250.
34. Nastala C.L., Edington H.D., McKinney T.G., Tahara H., Nalesnik M.A., Brunda M.J., et al. Recombinant IL-12 administration induces tumor regression in association with IFN-gamma production. J Immunol 1994, 153:1697-1706.
35. Colombo M.P., Trinchieri G. Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev 2002, 13:155-168.
36. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003, 3:133-146.
37. Tsung K., Dolan J.P., Tsung Y.L., Norton J.A. Macrophages as effector cells in interleukin 12-induced T cell-dependent tumor rejection. Cancer Res 2002, 62:5069-5075.
38. Schwartz Y., Avraham R., Benish M., Rosenne E., Ben-Eliyahu S. Prophylactic IL-12 treatment reduces postoperative metastasis: mediation by increased numbers but not cytotoxicity of NK cells. Breast Cancer Res Treat 2008, 107:211-223.
39. Sabel M.S., Su G., Griffith K.A., Chang A.E. Intratumoral delivery of encapsulated IL-12, IL-18 and TNF-alpha in a model of metastatic breast cancer. Breast Cancer Res Treat 2010, 122:325-336.
40. Cui J., Shin T., Kawano T., Sato H., Kondo E., Toura I., et al. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 1997, 278:1623-1626.
41. Smyth M.J., Taniguchi M., Street S.E. The anti-tumor activity of IL-12: mechanisms of innate immunity that are model and dose dependent. J Immunol 2000, 165:2665-2670.
42. Brunda M.J., Luistro L., Warrier R.R., Wright R.B., Hubbard B.R., Murphy M., et al. Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J Exp Med 1993, 178:1223-1230.
43. Noguchi Y., Richards E.C., Chen Y.T., Old L.J. Influence of interleukin 12 on p53 peptide vaccination against established Meth A sarcoma. Proc Natl Acad Sci U S A 1995, 92:2219-2223.
44. Gabrilovich D.I., Bronte V., Chen S.H., Colombo M.P., Ochoa A., Ostrand-Rosenberg S., et al. The terminology issue for myeloid-derived suppressor cells. Cancer Res 2007, 67:425.
45. Pastula A., Marcinkiewicz J. Myeloid-derived suppressor cells: a double-edged sword?. Int J Exp Pathol 2011, 92:73-78.
46. Nausch N., Galani I.E., Schlecker E., Cerwenka A. Mononuclear myeloid-derived " suppressor" cells express RAE-1 and activate natural killer cells. Blood 2008, 112:4080-4089.
47. Tomihara K., Guo M., Shin T., Sun X., Ludwig S.M., Brumlik M.J., et al. Antigen-specific immunity and cross-priming by epithelial ovarian carcinoma-induced CD11b(+)Gr-1(+) cells. J Immunol 2010, 184:6151-6160.
48. Sorlier P., Hartmann D.J., Denuziere A., Viton C., Domard A. Preparation and development of anti-chitosan antibodies. J Biomed Mater Res A 2003, 67:766-774.