Synergistic augmentation of CD40-mediated activation of antigen-presenting cells by amphiphilic poly(γ-glutamic acid) nanoparticles

Biomaterials

Volumn 33, Issue 26, 2012, Pages 6230-6239

  Broos, Sissela ^a   Sandin, Linda C ^b   Apel, Jenny ^a   Tötterman, Thomas H ^b   Akagi, Takami ^c   Akashi, Mitsuru ^c   Borrebaeck, Carl A K ^a   Ellmark, Peter ^a,d   Lindstedt, Malin ^a  

^a LUND UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c OSAKA UNIVERSITY   (Japan)

^d Alligator Bioscience AB   (Sweden)

Author keywords

Cell proliferation; Drug delivery; Immunostimulation; Nanoparticle; Protein adsorption

Indexed keywords

ADVERSE SIDE EFFECTS; AMPHIPHILICS; ANTIGEN PRESENTING CELLS; B CELLS; BLADDER CANCERS; CANCER IMMUNOTHERAPY; CYTOKINES; DRUG RETENTION; GLUTAMIC ACID; IMMUNOSTIMULATION; LIVER DAMAGE; MONOCLONAL ANTIBODIES (MABS); MULTIMERIZATION; PROLIFERATIVE EFFECTS; PROTEIN ADSORPTION; SERUM LEVELS; SIDE EFFECT; SYSTEMIC ADMINISTRATION; UP-REGULATION;

ADSORPTION; AMINO ACIDS; ANTIGENS; CELL PROLIFERATION; CHEMICAL ACTIVATION; DISEASES; DRUG DELIVERY; MEDICAL NANOTECHNOLOGY; MONOCLONAL ANTIBODIES;

NANOPARTICLES;

AMPHOPHILE; B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; FC RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NANOPARTICLE; POLY(GAMMA GLUTAMIC ACID); POLYMER; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADSORPTION; ANTIGEN PRESENTING CELL; ARTICLE; CELL ACTIVATION; CELL MATURATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE RELEASE; CYTOKINE RELEASE SYNDROME; DRUG RETENTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER INJURY; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD40; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; DRUG DELIVERY SYSTEMS; FEMALE; FLOW CYTOMETRY; HUMANS; MICE; NANOPARTICLES; POLYGLUTAMIC ACID; URINARY BLADDER NEOPLASMS;

EID: 84862867187     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.05.011     Document Type: Article

References (53)

1. Dunn G.P., Old L.J., Schreiber R.D. The three Es of cancer immunoediting. Annu Rev Immunol 2004, 22:329-360.
2. Sheng W.Y., Huang L. Cancer immunotherapy and nanomedicine. Pharm Res 2011, 28:200-214.
3. van Mierlo G.J., den Boer A.T., Medema J.P., van der Voort E.I., Fransen M.F., Offringa R., et al. CD40 stimulation leads to effective therapy of CD40(-) tumors through induction of strong systemic cytotoxic T lymphocyte immunity. Proc Natl Acad Sci U S A 2002, 99:5561-5566.
4. Tutt A.L., O'Brien L., Hussain A., Crowther G.R., French R.R., Glennie M.J. T cell immunity to lymphoma following treatment with anti-CD40 monoclonal antibody. J Immunol 2002, 168:2720-2728.
5. Vonderheide R.H., Flaherty K.T., Khalil M., Stumacher M.S., Bajor D.L., Hutnick N.A., et al. Clinical activity and immune modulation in cancer patients treated with CP-870,893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007, 25(7):876-883.
6. Advani R., Forero-Torres A., Furman R.R., Rosenblatt J.D., Younes A., Ren H., et al. Phase I study of the humanized anti-CD40 monoclonal antibody dacetuzumab in refractory or recurrent non-Hodgkin's lymphoma. J Clin Oncol 2009, 27:4371-4377.
7. Hussein M., Berenson J.R., Niesvizky R., Munshi N., Matous J., Sobecks R., et al. A phase I multidose study of dacetuzumab (SGN-40; humanized anti-CD40 monoclonal antibody) in patients with multiple myeloma. Haematologica 2010, 95:845-848.
8. Vonderheide R.H., Dutcher J.P., Anderson J.E., Eckhardt S.G., Stephans K.F., Razvillas B., et al. Phase I study of recombinant human CD40 ligand in cancer patients. J Clin Oncol 2001, 19:3280-3287.
9. Fransen M.F., Sluijter M., Morreau H., Arens R., Melief C.J. Local activation of CD8 T cells and systemic tumor eradication without toxicity via slow release and local delivery of agonistic CD40 antibody. Clin Cancer Res 2011, 17:2270-2280.
10. Kwong B., Liu H., Irvine D.J. Induction of potent anti-tumor responses while eliminating systemic side effects via liposome-anchored combinatorial immunotherapy. Biomaterials 2011, 32:5134-5147.
11. Akagi T., Kaneko T., Kida T., Akashi M. Preparation and characterization of biodegradable nanoparticles based on poly(gamma-glutamic acid) with l-phenylalanine as a protein carrier. J Contr Rel 2005, 108:226-236.
12. Himeno A., Akagi T., Uto T., Wang X., Baba M., Ibuki K., et al. Evaluation of the immune response and protective effects of rhesus macaques vaccinated with biodegradable nanoparticles carrying gp120 of human immunodeficiency virus. Vaccine 2010, 28:5377-5385.
13. Uto T., Wang X., Sato K., Haraguchi M., Akagi T., Akashi M., et al. Targeting of antigen to dendritic cells with poly(gamma-glutamic acid) nanoparticles induces antigen-specific humoral and cellular immunity. J Immunol 2007, 178:2979-2986.
14. Broos S., Lundberg K., Akagi T., Kadowaki K., Akashi M., Greiff L., et al. Immunomodulatory nanoparticles as adjuvants and allergen-delivery system to human dendritic cells: implications for specific immunotherapy. Vaccine 2010, 28:5075-5085.
15. Matsuo K., Ishii Y., Yoshinaga T., Akashi M., Mukai Y., Yoshioka Y., et al. The utility of poly(gamma-glutamic acid) nanoparticles as antigen delivery carriers in dendritic cell-based cancer immunotherapy. Biol Pharm Bull 2010, 33:2003-2007.
16. Lindstedt M., Johansson-Lindbom B., Borrebaeck C.A. Global reprogramming of dendritic cells in response to a concerted action of inflammatory mediators. Int Immunol 2002, 14:1203-1213.
17. Ellmark P., Andersson H., Abayneh S., Fenyo E.M., Borrebaeck C.A. Identification of a strongly activating human anti-CD40 antibody that suppresses HIV type 1 infection. AIDS Res Hum Retroviruses 2008, 24:367-373.
18. Tao M.H., Morrison S.L. Studies of aglycosylated chimeric mouse-human IgG. Role of carbohydrate in the structure and effector functions mediated by the human IgG constant region. J Immunol 1989, 143:2595-2601.
19. Li F., Ravetch J.V. Inhibitory Fcgamma receptor engagement drives adjuvant and anti-tumor activities of agonistic CD40 antibodies. Science 2011, 333:1030-1034.
20. Ellmark P., Ottosson C., Borrebaeck C.A., Malmborg Hager A.C., Furebring C. Modulation of the CD40-CD40 ligand interaction using human anti-CD40 single-chain antibody fragments obtained from the n-CoDeR phage display library. Immunology 2002, 106:456-463.
21. Uto T., Akagi T., Yoshinaga K., Toyama M., Akashi M., Baba M. The induction of innate and adaptive immunity by biodegradable poly(gamma-glutamic acid) nanoparticles via a TLR4 and MyD88 signaling pathway. Biomaterials 2011, 32:5206-5212.
22. Schultze J.L., Michalak S., Seamon M.J., Dranoff G., Jung K., Daley J., et al. CD40-activated human B cells: an alternative source of highly efficient antigen presenting cells to generate autologous antigen-specific T cells for adoptive immunotherapy. J Clin Invest 1997, 100:2757-2765.
23. Ranheim E.A., Kipps T.J. Activated T cells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal. J Exp Med 1993, 177:925-935.
24. Heufler C., Koch F., Stanzl U., Topar G., Wysocka M., Trinchieri G., et al. Interleukin-12 is produced by dendritic cells and mediates T helper 1 development as well as interferon-gamma production by T helper 1 cells. Eur J Immunol 1996, 26:659-668.
25. Xu M., Mizoguchi I., Morishima N., Chiba Y., Mizuguchi J., Yoshimoto T. Regulation of antitumor immune responses by the IL-12 family cytokines, IL-12, IL-23, and IL-27. Clin Dev Immunol 2010, 2010.
26. Macatonia S.E., Hosken N.A., Litton M., Vieira P., Hsieh C.S., Culpepper J.A., et al. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J Immunol 1995, 154:5071-5079.
27. Tahara H., Zitvogel L., Storkus W.J., Zeh H.J., McKinney T.G., Schreiber R.D., et al. Effective eradication of established murine tumors with IL-12 gene therapy using a polycistronic retroviral vector. J Immunol 1995, 154:6466-6474.
28. O'Donnell M.A., Luo Y., Hunter S.E., Chen X., Hayes L.L., Clinton S.K. Interleukin-12 immunotherapy of murine transitional cell carcinoma of the bladder: dose dependent tumor eradication and generation of protective immunity. J Urol 2004, 171:1330-1335.
29. 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.
30. Snijders A., Kalinski P., Hilkens C.M., Kapsenberg M.L. High-level IL-12 production by human dendritic cells requires two signals. Int Immunol 1998, 10:1593-1598.
31. Schulz O., Edwards A.D., Schito M., Aliberti J., Manickasingham S., Sher A., et al. CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 2000, 13:453-462.
32. Gladue R.P., Paradis T., Cole S.H., Donovan C., Nelson R., Alpert R., et al. The CD40 agonist antibody CP-870,893 enhances dendritic cell and B-cell activity and promotes anti-tumor efficacy in SCID-hu mice. Cancer Immunol Immunother 2011, 60:1009-1017.
33. Haswell L.E., Glennie M.J., Al-Shamkhani A. Analysis of the oligomeric requirement for signaling by CD40 using soluble multimeric forms of its ligand, CD154. Eur J Immunol 2001, 31:3094-3100.
34. Bishop G.A., Hostager B.S., Brown K.D. Mechanisms of TNF receptor-associated factor (TRAF) regulation in B lymphocytes. J Leukoc Biol 2002, 72:19-23.
35. Pullen S.S., Dang T.T., Crute J.J., Kehry M.R. CD40 signaling through tumor necrosis factor receptor-associated factors (TRAFs). Binding site specificity and activation of downstream pathways by distinct TRAFs. J Biol Chem 1999, 274:14246-14254.
36. Pullen S.S., Labadia M.E., Ingraham R.H., McWhirter S.M., Everdeen D.S., Alber T., et al. High-affinity interactions of tumor necrosis factor receptor-associated factors (TRAFs) and CD40 require TRAF trimerization and CD40 multimerization. Biochemistry 1999, 38:10168-10177.
37. Jalukar S.V., Hostager B.S., Bishop G.A. Characterization of the roles of TNF receptor-associated factor 6 in CD40-mediated B lymphocyte effector functions. J Immunol 2000, 164:623-630.
38. Baccam M., Bishop G.A. Membrane-bound CD154, but not CD40-specific antibody, mediates NF-kappaB-independent IL-6 production in B cells. Eur J Immunol 1999, 29:3855-3866.
39. Reyes-Moreno C., Girouard J., Lapointe R., Darveau A., Mourad W. CD40/CD40 homodimers are required for CD40-induced phosphatidylinositol 3-kinase-dependent expression of B7.2 by human B lymphocytes. J Biol Chem 2004, 279:7799-7806.
40. Kehry M.R., Castle B.E. Regulation of CD40 ligand expression and use of recombinant CD40 ligand for studying B cell growth and differentiation. Sem Immunol 1994, 6:287-294.
41. Fanslow W.C., Srinivasan S., Paxton R., Gibson M.G., Spriggs M.K., Armitage R.J. Structural characteristics of CD40 ligand that determine biological function. Sem Immunol 1994, 6:267-278.
42. Pound J.D., Challa A., Holder M.J., Armitage R.J., Dower S.K., Fanslow W.C., et al. Minimal cross-linking and epitope requirements for CD40-dependent suppression of apoptosis contrast with those for promotion of the cell cycle and homotypic adhesions in human B cells. Int Immunol 1999, 11:11-20.
43. Illum L., Jones P.D.E., Kreuter J., Baldwin R.W., Davis S.S. Adsorption of monoclonal antibodies to polyhexylcyanoacrylate nanoparticles and subsequent immunospecific binding to tumor cells in vitro. Int J Pharm 1983, 17:65-76.
44. Wiseman M.E., Frank C.W. Antibody adsorption and orientation on hydrophobic surfaces. Langmuir 2012, 28:1765-1774.
45. Zhou J., Tsao H.K., Sheng Y.J., Jiang S. Monte Carlo simulations of antibody adsorption and orientation on charged surfaces. J Chem Phys 2004, 121:1050-1057.
46. Jackaman C., Lew A.M., Zhan Y., Allan J.E., Koloska B., Graham P.T., et al. Deliberately provoking local inflammation drives tumors to become their own protective vaccine site. Int Immunol 2008, 20:1467-1479.
47. Kim Y.H., Gratzinger D., Harrison C., Brody J.D., Czerwinski D.K., Ai W.Z., et al. In situ vaccination against mycosis fungoides by intratumoral injection of a TLR9 agonist combined with radiation: a phase 1/2 study. Blood 2012, 119:355-363.
48. Dominguez A.L., Lustgarten J. Targeting the tumor microenvironment with anti-neu/anti-CD40 conjugated nanoparticles for the induction of antitumor immune responses. Vaccine 2010, 28:1383-1390.
49. Beatty G.L., Chiorean E.G., Fishman M.P., Saboury B., Teitelbaum U.R., Sun W., et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011, 331:1612-1616.
50. Nowak A.K., Robinson B.W., Lake R.A. Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res 2003, 63:4490-4496.
51. Honeychurch J., Glennie M.J., Johnson P.W., Illidge T.M. Anti-CD40 monoclonal antibody therapy in combination with irradiation results in a CD8 T-cell-dependent immunity to B-cell lymphoma. Blood 2003, 102:1449-1457.
52. Ahonen C.L., Doxsee C.L., McGurran S.M., Riter T.R., Wade W.F., Barth R.J., et al. Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN. J Exp Med 2004, 199:775-784.
53. Uno T., Takeda K., Kojima Y., Yoshizawa H., Akiba H., Mittler R.S., et al. Eradication of established tumors in mice by a combination antibody-based therapy. Nat Med 2006, 12:693-698.