Reprogramming the lung microenvironment by inhaled immunotherapy fosters immune destruction of tumor

OncoImmunology

Volumn 5, Issue 11, 2016, Pages

  Le Noci, Valentino ^a,b   Sommariva, Michele ^a,b   Tortoreto, Monica ^c   Zaffaroni, Nadia ^c   Campiglio, Manuela ^b   Tagliabue, Elda ^b   Balsari, Andrea ^a,b   Sfondrini, Lucia ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b Molecular Targeting Unit   (Italy)

^c NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

IFN ; inhalation therapy; lung microenvironment; TLR agonists; tumor

Indexed keywords

ALPHA INTERFERON; ARG 1 PROTEIN; CD69 ANTIGEN; CELL SURFACE MARKER; CPG OLIGODEOXYNUCLEOTIDE ANTIBODY; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 15; MEMBRANE PROTEIN; MESSENGER RNA; MONOCLONAL ANTIBODY; RB6 8C5 ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; CYTOTOXICITY ASSAY; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; LUNG METASTASIS; MACROPHAGE; MELANOMA; MOUSE; MYELOID DERIVED SUPPRESSIVE CELL; NATURAL KILLER; NEBULIZATION; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SUPPRESSOR CELL; TREATMENT OUTCOME; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

EID: 84994181514     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1234571     Document Type: Article

References (33)

1. Keskinov AA, Shurin MR. Myeloid regulatory cells in tumor spreading and metastasis. Immunobiology 2015; 220:236–42; PMID:25178934; doi:10.1016/j.imbio.2014.07.017
2. Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol 2009; 182:240–9; PMID:19109155; doi:10.4049/jimmunol.182.1.240
3. Elkabets M, Ribeiro VS, Dinarello CA, Ostrand-Rosenberg S, Di Santo JP, Apte RN, Vosshenrich CA. IL-1beta regulates a novel myeloid-derived suppressor cell subset that impairs NK cell development and function. Eur J Immunol 2010; 40:3347–57; PMID:21110318; doi:10.1002/eji.201041037
4. Liu C, Yu S, Kappes J, Wang J, Grizzle WE, Zinn KR, Zhang HG. Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host. Blood 2007; 109:4336–42; PMID:17244679; doi:10.1182/blood-2006-09-046201
5. Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, Lehner F, Manns MP, Greten TF, Korangy F. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009; 50:799–807; PMID:19551844; doi:10.1002/hep.23054
6. Ostrand-Rosenberg S, Sinha P, Beury DW, Clements VK. Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin Cancer Biol 2012; 22:275–81; PMID:22313874; doi:10.1016/j.semcancer.2012.01.011
7. Le Noci V, Tortoreto M, Gulino A, Storti C, Bianchi F, Zaffaroni N, Tripodo C, Tagliabue E, Balsari A, Sfondrini L. Poly(I:C) and CpG-ODN combined aerosolization to treat lung metastases and counter the immunosuppressive microenvironment. OncoImmunology 2015; 4(10):e1040214; PMID:26451303; doi:10.1080/2162402X.2015.1040214
8. Trinchieri G, Santoli D. Anti-viral activity induced by culturing lymphocytes with tumor-derived or virus-transformed cells. Enhancement of human natural killer cell activity by interferon and antagonistic inhibition of susceptibility of target cells to lysis. J Exp Med 1978; 147:1314–33; PMID:650156
9. Karimi K, Karimi Y, Chan J, Boudreau JE, Basset J, Chew MV, Reid S, Bramson JL, Wan Y, Ashkar AA. Type I IFN signaling on dendritic cells is required for NK cell-mediated anti-tumor immunity. Innate Immun 2015; 21:626–34; PMID:25749844; doi:10.1177/1753425915575078
10. Zhuang PY, Shen J, Zhu XD, Zhang JB, Tang ZY, Qin LX, Sun HC. Direct transformation of lung microenvironment by interferon-alpha treatment counteracts growth of lung metastasis of hepatocellular carcinoma. PLoS One 2013; 8:e58913; PMID:23527047; doi:10.1371/journal.pone.0058913
11. Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, Sloan EK, Parker BS, Bowtell DD, Smyth MJ, et al. Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res 2012; 72:3906–11; PMID:22751463; doi:10.1158/0008-5472.CAN-11-3873
12. Schlecker E, Stojanovic A, Eisen C, Quack C, Falk CS, Umansky V, Cerwenka A. Tumor-infiltrating monocytic myeloid-derived suppressor cells mediate CCR5-dependent recruitment of regulatory T cells favoring tumor growth. J Immunol 2012; 189:5602–11; PMID:23152559; doi:10.4049/jimmunol.1201018
13. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008; 181:5791–802; PMID:18832739; doi:10.4049/jimmunol.181.8.5791
14. Saiwai H, Kumamaru H, Ohkawa Y, Kubota K, Kobayakawa K, Yamada H, Yokomizo T, Iwamoto Y, Okada S. Ly6C+ Ly6G- myeloid-derived suppressor cells play a critical role in the resolution of acute inflammation and the subsequent tissue repair process after spinal cord injury. J Neurochem 2013; 125:74–88; PMID:23278273; doi:10.1111/jnc.12135
15. Mattiola I, Pesant M, Tentorio PF, Molgora M, Marcenaro E, Lugli E, Locati M, Mavilio D. Priming of human resting NK cells by autologous M1 macrophages via the engagement of IL-1beta, IFN-beta, and IL-15 pathways. J Immunol 2015; 195:2818–28; PMID:26276870; doi:10.4049/jimmunol.1500325
16. Kaisho T, Akira S. Toll-like receptors as adjuvant receptors. Biochim Biophys Acta 2002; 1589:1–13; PMID:11909637; doi:10.1016/S0167-4889(01)00182-3
17. Hervas-Stubbs S, Perez-Gracia JL, Rouzaut A, Sanmamed MF, Le BA, Melero I. Direct effects of type I interferons on cells of the immune system. Clin Cancer Res 2011; 17:2619–27; PMID:21372217; doi:10.1158/1078-0432.CCR-10-1114
18. Trinchieri G. Type I interferon:friend or foe? J Exp Med 2010; 207:2053–63; PMID:20837696; doi:10.1084/jem.20101664
19. Srivastava MK, Zhu L, Harris-White M, Kar UK, Huang M, Johnson MF, Lee JM, Elashoff D, Strieter R, Dubinett S, Sharma S. Myeloid suppressor cell depletion augments antitumor activity in lung cancer. PLoS One 2012; 7:e40677; PMID:22815789; doi:10.1371/journal.pone.0040677
20. Ribechini E, Leenen PJ, Lutz MB. Gr-1 antibody induces STAT signaling, macrophage marker expression and abrogation of myeloid-derived suppressor cell activity in BM cells. Eur J Immunol 2009; 39:3538–51; PMID:19830733; doi:10.1002/eji.200939530
21. Ma C, Greten TF. Editorial:“Invisible” MDSC in tumor-bearing individuals after antibody depletion:fact or fiction? J Leukoc Biol 2016; 99:794–047; PMID:27252522; doi:10.1189/jlb.5CE0116-047R
22. Guilleminault L, Azzopardi N, Arnoult C, Sobilo J, Herve V, Montharu J, Guillon A, Andres C, Herault O, Le PA, et al. Fate of inhaled monoclonal antibodies after the deposition of aerosolized particles in the respiratory system. J Control Release 2014; 196:344–54; PMID:25451545; doi:10.1016/j.jconrel.2014.10.003
23. Leyva-Grado VH, Tan GS, Leon PE, Yondola M, Palese P. Direct administration in the respiratory tract improves efficacy of broadly neutralizing anti-influenza virus monoclonal antibodies. Antimicrob Agents Chemother 2015; 59:4162–72; PMID:25941218; doi:10.1128/AAC.00290-15
24. Herve V, Rabbe N, Guilleminault L, Paul F, Schlick L, Azzopardi N, Duruisseaux M, Fouquenet D, Montharu J, Redini F, et al. VEGF neutralizing aerosol therapy in primary pulmonary adenocarcinoma with K-ras activating-mutations. MAbs 2014; 6:1638–48; PMID:25484066; doi:10.4161/mabs.34454
25. Jonasch E, Haluska FG. Interferon in oncological practice:review of interferon biology, clinical applications, and toxicities. Oncologist 2001; 6:34–55; PMID:11161227; doi:10.1634/theoncologist.6-1-34
26. Giosue S, Casarini M, Ameglio F, Zangrilli P, Palla M, Altieri AM, Bisetti A. Aerosolized interferon-alpha treatment in patients with multi-drug-resistant pulmonary tuberculosis. Eur Cytokine Netw 2000; 11:99–104; PMID:10705306
27. van Zandwijk N, Jassem E, Dubbelmann R, Braat MC, Rumke P. Aerosol application of interferon-alpha in the treatment of bronchioloalveolar carcinoma. Eur J Cancer 1990; 26:738–40; PMID:2168195
28. Kinnula V, Cantell K, Mattson K. Effect of inhaled natural interferon-alpha on diffuse bronchioalveolar carcinoma. Eur J Cancer 1990; 26:740–1; PMID:2168196
29. Brown L, Roda J, Terrell C, Chaudhury AR, Crespin T, Carson WE, Lesinski GB. Interferon alpha and CPG oligodeoxynucleotides elicit additive immunostimulatory and antitumor effects. Surgery 2006; 140:297–306; PMID:16904983; doi:10.1016/j.surg.2006.05.005
30. Hiraide A, Hiroishi K, Eguchi J, Ishii S, Doi H, Imawari M. Dendritic cells stimulated with cytidine-phosphate-guanosine oligodeoxynucleotides and interferon-alpha-expressing tumor cells effectively reduce outgrowth of established tumors in vivo. Cancer Sci 2008; 99:1663–9; PMID:18754881; doi:10.1111/j.1349-7006.2008.00858.x
31. Sfondrini L, Sommariva M, Tortoreto M, Meini A, Piconese S, Calvaruso M, Van RN, Bonecchi R, Zaffaroni N, Colombo MP, et al. Anti-tumor activity of CpG-ODN aerosol in mouse lung metastases. Int J Cancer 2013; 133:383–93; PMID:23319306; doi:10.1002/ijc.28028
32. Bivas-Benita M, Zwier R, Junginger HE, Borchard G. Non-invasive pulmonary aerosol delivery in mice by the endotracheal route. Eur J Pharm Biopharm 2005; 61:214–8; doi:10.1016/j.ejpb.2005.04.009
33. Storti C, Le Noci V, Sommariva M, Tagliabue E, Balsari A, Sfondrini L. Aerosol delivery in the treatment of lung cance. Curr Cancer Drug Targets 2015; 15(7):604–12; PMID:26033086