Tumor Vasculature Targeted TNFα Therapy: Reversion of Microenvironment Anergy and Enhancement of the Anti-tumor Efficiency

Author(s): Enrica Balza, Barbara Carnemolla, Paola Orecchia, Anna Rubartelli, Alessandro Poggi, Lorenzo Mortara*

Journal Name: Current Medicinal Chemistry

Volume 27 , Issue 25 , 2020


  Journal Home
Translate in Chinese
Become EABM
Become Reviewer
Call for Editor

Abstract:

Tumor cells and tumor-associated stromal cells such as immune, endothelial and mesenchimal cells create a Tumor Microenvironment (TME) which allows tumor cell promotion, growth and dissemination while dampening the anti-tumor immune response. Efficient anti-tumor interventions have to keep into consideration the complexity of the TME and take advantage of immunotherapy and chemotherapy combined approaches. Thus, the aim of tumor therapy is to directly hit tumor cells and reverse endothelial and immune cell anergy. Selective targeting of tumor vasculature using TNFα-associated peptides or antibody fragments in association with chemotherapeutic agents, has been shown to exert a potent stimulatory effect on endothelial cells as well as on innate and adaptive immune responses. These drug combinations reducing the dose of single agents employed have led to minimize the associated side effects. In this review, we will analyze different TNFα-mediated tumor vesseltargeted therapies in both humans and tumor mouse models, with emphasis on the role played by the cross-talk between natural killer and dendritic cells and on the ability of TNFα to trigger tumor vessel activation and normalization. The improvement of the TNFα-based therapy with anti-angiogenic immunomodulatory drugs that may convert the TME from immunosuppressive to immunostimulant, will be discussed as well.

Keywords: Tumor vasculature, TNFα, targeting immunotherapy, chemotherapy, L19, NK cells, dendritic cells, Tcell response.

[1]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: the next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[2]
Albini, A.; Bruno, A.; Noonan, D.M.; Mortara, L. Contribution to tumor angiogenesis from innate immune cells within the tumor microenvironment: Implications for immunotherapies. Front. Immunol., 2018, 9, 527.
[http://dx.doi.org/10.3389/fimmu.2018.00527] [PMID: 29675018]
[3]
Poggi, A.; Varesano, S.; Zocchi, M.R. How to Hit Mesenchymal Stromal Cells and Make the Tumor Microenvironment Immunostimulant Rather Than Immunosuppressive. Front. Immunol., 2018, 9, 262.
[http://dx.doi.org/10.3389/fimmu.2018.00262] [PMID: 29515580]
[4]
Joyce, J.A.; Pollard, J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer, 2009, 9(4), 239-252.
[http://dx.doi.org/10.1038/nrc2618] [PMID: 19279573]
[5]
Coussens, L.M.; Zitvogel, L.; Palucka, A.K. Neutralizing tumor-promoting chronic inflammation: a magic bullet? Science, 2013, 339(6117), 286-291.
[http://dx.doi.org/10.1126/science.1232227] [PMID: 23329041]
[6]
Bruno, A.; Focaccetti, C.; Pagani, A.; Imperatori, A.S.; Spagnoletti, M.; Rotolo, N.; Cantelmo, A.R.; Franzi, F.; Capella, C.; Ferlazzo, G.; Mortara, L.; Albini, A.; Noonan, D.M. The proangiogenic phenotype of natural killer cells in patients with non-small cell lung cancer. Neoplasia, 2013, 15(2), 133-142.
[http://dx.doi.org/10.1593/neo.121758] [PMID: 23441128]
[7]
Porta, C.; Sica, A.; Riboldi, E. Tumor-associated myeloid cells: new understandings on their metabolic regulation and their influence in cancer immunotherapy. FEBS J., 2017.
[http://dx.doi.org/10.1111/febs.14288] [PMID: 28985035]
[8]
Noonan, D.M.; De Lerma Barbaro, A.; Vannini, N.; Mortara, L.; Albini, A. Inflammation, inflammatory cells and angiogenesis: decisions and indecisions. Cancer Metastasis Rev., 2008, 27(1), 31-40.
[http://dx.doi.org/10.1007/s10555-007-9108-5] [PMID: 18087678]
[9]
Bruno, A.; Pagani, A.; Pulze, L.; Albini, A.; Dallaglio, K.; Noonan, D.M.; Mortara, L. Orchestration of angiogenesis by immune cells. Front. Oncol., 2014, 4, 131.
[http://dx.doi.org/10.3389/fonc.2014.00131] [PMID: 25072019]
[10]
De Palma, M.; Biziato, D.; Petrova, T.V. Microenvironmental regulation of tumour angiogenesis. Nat. Rev. Cancer, 2017, 17(8), 457-474.
[http://dx.doi.org/10.1038/nrc.2017.51] [PMID: 28706266]
[11]
Mortara, L.; Benest, A.V.; Bates, D.O.; Noonan, D.M. Can the co-dependence of the immune system and angiogenesis facilitate pharmacological targeting of tumours? Curr. Opin. Pharmacol., 2017, 35, 66-74.
[http://dx.doi.org/10.1016/j.coph.2017.05.009] [PMID: 28623714]
[12]
Parisi, L.; Gini, E.; Baci, D.; Tremolati, M.; Fanuli, M.; Bassani, B.; Farronato, G.; Bruno, A.; Mortara, L. Macrophage polarization in chronic inflammatory diseases: killers or builders? J. Immunol. Res., 2018, 20188917804
[http://dx.doi.org/10.1155/2018/8917804]] [PMID: 29507865]
[13]
Baxevanis, C.N.; Perez, S.A.; Papamichail, M. Cancer immunotherapy. Crit. Rev. Clin. Lab. Sci., 2009, 46(4), 167-189.
[http://dx.doi.org/10.1080/10408360902937809] [PMID: 19650714]
[14]
Dougan, M.; Dranoff, G. Immune therapy for cancer. Annu. Rev. Immunol., 2009, 27, 83-117.
[http://dx.doi.org/10.1146/annurev.immunol.021908.132544] [PMID: 19007331]
[15]
Mancuso, A.; Sternberg, C.N. New treatments for metastatic kidney cancer. Can. J. Urol., 2005, 12(Suppl. 1), 66-70.
[PMID: 15780170]
[16]
Zohar, S.; Medioni, J.; Lebbé, C.; Avril, M.F.; Kerob, D.; Eftekhari, P.; Driheme, A.; Lebras, K.C.; Bruzzoni-Giovanelli, H.; Levy, V.; Chevret, S.; Calvo, F. Interest in an original methodology to define the optimal dosage of interferon-alpha-2a in metastatic melanoma patients. Melanoma Res., 2009, 19(6), 379-384.
[http://dx.doi.org/10.1097/CMR.0b013e3283281042] [PMID: 19858763]
[17]
Hudak, L.; Tezeeh, P.; Wedel, S.; Makarević, J.; Juengel, E.; Tsaur, I.; Bartsch, G.; Wiesner, C.; Haferkamp, A.; Blaheta, R.A. Low dosed interferon alpha augments the anti-tumor potential of histone deacetylase inhibition on prostate cancer cell growth and invasion. Prostate, 2012, 72(16), 1719-1735.
[http://dx.doi.org/10.1002/pros.22525] [PMID: 22473339]
[18]
Shaker, M.A.; Younes, H.M. Interleukin-2: evaluation of routes of administration and current delivery systems in cancer therapy. J. Pharm. Sci., 2009, 98(7), 2268-2298.
[http://dx.doi.org/10.1002/jps.21596] [PMID: 19009549]
[19]
Papadia, F.; Basso, V.; Patuzzo, R.; Maurichi, A.; Di Florio, A.; Zardi, L.; Ventura, E.; González-Iglesias, R.; Lovato, V.; Giovannoni, L.; Tasciotti, A.; Neri, D.; Santinami, M.; Menssen, H.D.; De Cian, F. Isolated limb perfusion with the tumor-targeting human monoclonal antibody-cytokine fusion protein L19-TNF plus melphalan and mild hyperthermia in patients with locally advanced extremity melanoma. J. Surg. Oncol., 2013, 107(2), 173-179.
[http://dx.doi.org/10.1002/jso.23168] [PMID: 22674435]
[20]
Danielli, R.; Patuzzo, R.; Di Giacomo, A.M.; Gallino, G.; Maurichi, A.; Di Florio, A.; Cutaia, O.; Lazzeri, A.; Fazio, C.; Miracco, C.; Giovannoni, L.; Elia, G.; Neri, D.; Maio, M.; Santinami, M. Intralesional administration of L19-IL2/L19-TNF in stage III or stage IVM1a melanoma patients: results of a phase II study. Cancer Immunol. Immunother., 2015, 64(8), 999-1009.
[http://dx.doi.org/10.1007/s00262-015-1704-6] [PMID: 25971540]
[21]
Eggermont, A.M.; Schraffordt Koops, H.; Klausner, J.M.; Schlag, P.M.; Kroon, B.B.; Ben-Ari, G.; Lejeune, F.J. Isolated limb perfusion with high-dose tumor necrosis factor-alpha for locally advanced extremity soft tissue sarcomas.Cancer Treat. Res.,, 1997, 91, pp. 189-203.
[http://dx.doi.org/10.1007/978-1-4615-6121-7_13] [PMID: 9286497]
[22]
Carswell, E.A.; Old, L.J.; Kassel, R.L.; Green, S.; Fiore, N.; Williamson, B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc. Natl. Acad. Sci. USA, 1975, 72(9), 3666-3670.
[http://dx.doi.org/10.1073/pnas.72.9.3666] [PMID: 1103152]
[23]
Liénard, D.; Eggermont, A.M.; Schraffordt Koops, H.; Kroon, B.B.; Rosenkaimer, F.; Autier, P.; Lejeune, F.J. Isolated perfusion of the limb with high-dose tumour necrosis factor-alpha (TNF-alpha), interferon-gamma (IFN-gamma) and melphalan for melanoma stage III. Results of a multi-centre pilot study. Melanoma Res., 1994, 4(Suppl. 1), 21-26.
[PMID: 8038591]
[24]
Balkwill, F. TNF-alpha in promotion and progression of cancer. Cancer Metastasis Rev., 2006, 25(3), 409-416.
[http://dx.doi.org/10.1007/s10555-006-9005-3] [PMID: 16951987]
[25]
Balza, E.; Mortara, L.; Sassi, F.; Monteghirfo, S.; Carnemolla, B.; Castellani, P.; Neri, D.; Accolla, R.S.; Zardi, L.; Borsi, L. Targeted delivery of tumor necrosis factor-alpha to tumor vessels induces a therapeutic T cell-mediated immune response that protects the host against syngeneic tumors of different histologic origin. Clinical cancer research: an official journal of the American Association for Cancer Research, 2006, 12(8), 2575-2582.
[26]
Mortara, L.; Balza, E.; Sassi, F.; Castellani, P.; Carnemolla, B.; De Lerma Barbaro, A.; Fossati, S.; Tosi, G.; Accolla, R.S.; Borsi, L. Therapy-induced antitumor vaccination by targeting tumor necrosis factor alpha to tumor vessels in combination with melphalan. Eur. J. Immunol., 2007, 37(12), 3381-3392.
[http://dx.doi.org/10.1002/eji.200737450] [PMID: 18022863]
[27]
Balza, E.; Zanellato, S.; Poggi, A.; Reverberi, D.; Rubartelli, A.; Mortara, L. The therapeutic T-cell response induced by tumor delivery of TNF and melphalan is dependent on early triggering of natural killer and dendritic cells. Eur. J. Immunol., 2017, 47(4), 743-753.
[http://dx.doi.org/10.1002/eji.201646544] [PMID: 28198545]
[28]
Mortara, L.; Orecchia, P.; Castellani, P.; Borsi, L.; Carnemolla, B.; Balza, E. Schedule-dependent therapeutic efficacy of L19mTNF-α and melphalan combined with gemcitabine. Cancer Med., 2013, 2(4), 478-487.
[http://dx.doi.org/10.1002/cam4.89] [PMID: 24156020]
[29]
Balza, E.; Carnemolla, B.; Mortara, L.; Castellani, P.; Soncini, D.; Accolla, R.S.; Borsi, L. Therapy-induced antitumor vaccination in neuroblastomas by the combined targeting of IL-2 and TNFalpha. Int. J. Cancer, 2010, 127(1), 101-110.
[http://dx.doi.org/10.1002/ijc.25018] [PMID: 19877124]
[30]
Schrama, D.; Reisfeld, R.A.; Becker, J.C. Antibody targeted drugs as cancer therapeutics. Nat. Rev. Drug Discov., 2006, 5(2), 147-159.
[http://dx.doi.org/10.1038/nrd1957] [PMID: 16424916]
[31]
Neri, D.; Sondel, P.M. Immunocytokines for cancer treatment: past, present and future. Curr. Opin. Immunol., 2016, 40, 96-102.
[http://dx.doi.org/10.1016/j.coi.2016.03.006] [PMID: 27060634]
[32]
Bemelmans, M.H.; van Tits, L.J.; Buurman, W.A. Tumor necrosis factor: function, release and clearance. Crit. Rev. Immunol., 1996, 16(1), 1-11.
[http://dx.doi.org/10.1615/CritRevImmunol.v16.i1.10] [PMID: 8809470]
[33]
Briscoe, D.M.; Cotran, R.S.; Pober, J.S. Effects of tumor necrosis factor, lipopolysaccharide, and IL-4 on the expression of vascular cell adhesion molecule-1 in vivo. Correlation with CD3+ T cell infiltration. J. Immunol., 1992, 149(9), 2954-2960.
[PMID: 1383333]
[34]
Fiedler, U.; Reiss, Y.; Scharpfenecker, M.; Grunow, V.; Koidl, S.; Thurston, G.; Gale, N.W.; Witzenrath, M.; Rosseau, S.; Suttorp, N.; Sobke, A.; Herrmann, M.; Preissner, K.T.; Vajkoczy, P.; Augustin, H.G. Angiopoietin-2 sensitizes endothelial cells to TNF-alpha and has a crucial role in the induction of inflammation. Nat. Med., 2006, 12(2), 235-239.
[http://dx.doi.org/10.1038/nm1351] [PMID: 16462802]
[35]
Curnis, F.; Sacchi, A.; Corti, A. Improving chemotherapeutic drug penetration in tumors by vascular targeting and barrier alteration. J. Clin. Invest., 2002, 110(4), 475-482.
[http://dx.doi.org/10.1172/JCI0215223] [PMID: 12189241]
[36]
Bertilaccio, M.T.; Grioni, M.; Sutherland, B.W.; Degl’Innocenti, E.; Freschi, M.; Jachetti, E.; Greenberg, N.M.; Corti, A.; Bellone, M. Vasculature-targeted tumor necrosis factor-alpha increases the therapeutic index of doxorubicin against prostate cancer. Prostate, 2008, 68(10), 1105-1115.
[http://dx.doi.org/10.1002/pros.20775] [PMID: 18437689]
[37]
Marchiò, S.; Lahdenranta, J.; Schlingemann, R.O.; Valdembri, D.; Wesseling, P.; Arap, M.A.; Hajitou, A.; Ozawa, M.G.; Trepel, M.; Giordano, R.J.; Nanus, D.M.; Dijkman, H.B.; Oosterwijk, E.; Sidman, R.L.; Cooper, M.D.; Bussolino, F.; Pasqualini, R.; Arap, W. Aminopeptidase A is a functional target in angiogenic blood vessels. Cancer Cell, 2004, 5(2), 151-162.
[http://dx.doi.org/10.1016/S1535-6108(04)00025-X] [PMID: 14998491]
[38]
Pasqualini, R.; Koivunen, E.; Kain, R.; Lahdenranta, J.; Sakamoto, M.; Stryhn, A.; Ashmun, R.A.; Shapiro, L.H.; Arap, W.; Ruoslahti, E. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res., 2000, 60(3), 722-727.
[PMID: 10676659]
[39]
Loi, M.; Marchio, S.; Becherini, P.; Di Paolo, D.; Soster, M.; Curnis, F.; Brignole, C.; Pagnan, G.; Perri, P.; Caffa, I.; Longhi, R.; Nico, B.; Bussolino, F.; Gambini, C.; Ribatti, D.; Cilli, M.; Arap, W.; Pasqualini, R.; Allen, T.M.; Corti, A.; Ponzoni, M.; Pastorino, F. Combined targeting of perivascular and endothelial tumor cells enhances anti-tumor efficacy of liposomal chemotherapy in neuroblastoma. Journal of controlled release : official journal of the Controlled Release Society, 2010, 145(1), 66-73.
[http://dx.doi.org/10.1016/j.jconrel.2010.03.015]
[40]
Mueller, J.; Gaertner, F.C.; Blechert, B.; Janssen, K.P.; Essler, M. Targeting of tumor blood vessels: a phage-displayed tumor-homing peptide specifically binds to matrix metalloproteinase-2-processed collagen IV and blocks angiogenesis in vivo. Mol. Cancer Res., 2009, 7(7), 1078-1085.
[http://dx.doi.org/10.1158/1541-7786.MCR-08-0538] [PMID: 19584266]
[41]
Pasqualini, R.; Koivunen, E.; Ruoslahti, E. Alpha v integrins as receptors for tumor targeting by circulating ligands. Nat. Biotechnol., 1997, 15(6), 542-546.
[http://dx.doi.org/10.1038/nbt0697-542] [PMID: 9181576]
[42]
Corti, A.; Curnis, F.; Arap, W.; Pasqualini, R. The neovasculature homing motif NGR: more than meets the eye. Blood, 2008, 112(7), 2628-2635.
[http://dx.doi.org/10.1182/blood-2008-04-150862] [PMID: 18574027]
[43]
Curnis, F.; Arrigoni, G.; Sacchi, A.; Fischetti, L.; Arap, W.; Pasqualini, R.; Corti, A. Differential binding of drugs containing the NGR motif to CD13 isoforms in tumor vessels, epithelia, and myeloid cells. Cancer Res., 2002, 62(3), 867-874.
[PMID: 11830545]
[44]
Calcinotto, A.; Grioni, M.; Jachetti, E.; Curnis, F.; Mondino, A.; Parmiani, G.; Corti, A.; Bellone, M. Targeting TNF-α to neoangiogenic vessels enhances lymphocyte infiltration in tumors and increases the therapeutic potential of immunotherapy. J. Immunol., 2012, 188(6), 2687-2694.
[http://dx.doi.org/10.4049/jimmunol.1101877] [PMID: 22323546]
[45]
Gregorc, V.; Santoro, A.; Bennicelli, E.; Punt, C.J.; Citterio, G.; Timmer-Bonte, J.N.; Caligaris Cappio, F.; Lambiase, A.; Bordignon, C.; van Herpen, C.M. Phase Ib study of NGR-hTNF, a selective vascular targeting agent, administered at low doses in combination with doxorubicin to patients with advanced solid tumours. Br. J. Cancer, 2009, 101(2), 219-224.
[http://dx.doi.org/10.1038/sj.bjc.6605162] [PMID: 19568235]
[46]
Gregorc, V.; Zucali, P.A.; Santoro, A.; Ceresoli, G.L.; Citterio, G.; De Pas, T.M.; Zilembo, N.; De Vincenzo, F.; Simonelli, M.; Rossoni, G.; Spreafico, A.; Grazia Viganò, M.; Fontana, F.; De Braud, F.G.; Bajetta, E.; Caligaris-Cappio, F.; Bruzzi, P.; Lambiase, A.; Bordignon, C. Phase II study of asparagine-glycine-arginine-human tumor necrosis factor alpha, a selective vascular targeting agent, in previously treated patients with malignant pleural mesothelioma. J. Clin. Oncol., 2010, 28(15), 2604-2611.
[http://dx.doi.org/10.1200/JCO.2009.27.3649] [PMID: 20406925]
[47]
Manzo, T.; Sturmheit, T.; Basso, V.; Petrozziello, E.; Hess Michelini, R.; Riba, M.; Freschi, M.; Elia, A.R.; Grioni, M.; Curnis, F.; Protti, M.P.; Schumacher, T.N.; Debets, R.; Swartz, M.A.; Corti, A.; Bellone, M.; Mondino, A. T Cells Redirected to a Minor Histocompatibility Antigen Instruct Intratumoral TNFα Expression and Empower Adoptive Cell Therapy for Solid Tumors. Cancer Res., 2017, 77(3), 658-671.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-0725] [PMID: 27872095]
[48]
Santimaria, M.; Moscatelli, G.; Viale, G.L.; Giovannoni, L.; Neri, G.; Viti, F.; Leprini, A.; Borsi, L.; Castellani, P.; Zardi, L.; Neri, D.; Riva, P. Immunoscintigraphic detection of the ED-B domain of fibronectin, a marker of angiogenesis, in patients with cancer. Clinical cancer research : an official journal of the American Association for Cancer Research,, 2003, 9(2), 571-579.
[49]
Tarli, L.; Balza, E.; Viti, F.; Borsi, L.; Castellani, P.; Berndorff, D.; Dinkelborg, L.; Neri, D.; Zardi, L. A high-affinity human antibody that targets tumoral blood vessels. Blood, 1999, 94(1), 192-198.
[http://dx.doi.org/10.1182/blood.V94.1.192.413k22_192_198] [PMID: 10381513]
[50]
Castellani, P.; Viale, G.; Dorcaratto, A.; Nicolo, G.; Kaczmarek, J.; Querze, G.; Zardi, L. The fibronectin isoform containing the ED-B oncofetal domain: a marker of angiogenesis. Int. J. Cancer, 1994, 59(5), 612-618.
[http://dx.doi.org/10.1002/ijc.2910590507] [PMID: 7525495]
[51]
Borsi, L.; Balza, E.; Carnemolla, B.; Sassi, F.; Castellani, P.; Berndt, A.; Kosmehl, H.; Biro, A.; Siri, A.; Orecchia, P.; Grassi, J.; Neri, D.; Zardi, L. Selective targeted delivery of TNFalpha to tumor blood vessels. Blood, 2003, 102(13), 4384-4392.
[http://dx.doi.org/10.1182/blood-2003-04-1039] [PMID: 12933583]
[52]
Schwager, K.; Hemmerle, T.; Aebischer, D.; Neri, D. The immunocytokine L19-IL2 eradicates cancer when used in combination with CTLA-4 blockade or with L19-TNF. J. Invest. Dermatol., 2013, 133(3), 751-758.
[http://dx.doi.org/10.1038/jid.2012.376] [PMID: 23096716]
[53]
Hemmerle, T.; Probst, P.; Giovannoni, L.; Green, A.J.; Meyer, T.; Neri, D. The antibody-based targeted delivery of TNF in combination with doxorubicin eradicates sarcomas in mice and confers protective immunity. Br. J. Cancer, 2013, 109(5), 1206-1213.
[http://dx.doi.org/10.1038/bjc.2013.421] [PMID: 23887603]
[54]
Spitaleri, G.; Berardi, R.; Pierantoni, C.; De Pas, T.; Noberasco, C.; Libbra, C.; González-Iglesias, R.; Giovannoni, L.; Tasciotti, A.; Neri, D.; Menssen, H.D.; de Braud, F. Phase I/II study of the tumour-targeting human monoclonal antibody-cytokine fusion protein L19-TNF in patients with advanced solid tumours. J. Cancer Res. Clin. Oncol., 2013, 139(3), 447-455.
[http://dx.doi.org/10.1007/s00432-012-1327-7] [PMID: 23160853]
[55]
Ziffels, B.; Pretto, F.; Neri, D. Intratumoral administration of IL2- and TNF-based fusion proteins cures cancer without establishing protective immunity. Immunotherapy, 2018, 10(3), 177-188.
[http://dx.doi.org/10.2217/imt-2017-0119] [PMID: 29370721]
[56]
Koonce, N.A.; Quick, C.M.; Hardee, M.E.; Jamshidi-Parsian, A.; Dent, J.A.; Paciotti, G.F.; Nedosekin, D.; Dings, R.P.; Griffin, R.J. Combination of Gold Nanoparticle-Conjugated Tumor Necrosis Factor-α and Radiation Therapy Results in a Synergistic Antitumor Response in Murine Carcinoma Models. Int. J. Radiat. Oncol. Biol. Phys., 2015, 93(3), 588-596.
[http://dx.doi.org/10.1016/j.ijrobp.2015.07.2275] [PMID: 26461001]
[57]
Curnis, F.; Fiocchi, M.; Sacchi, A.; Gori, A.; Gasparri, A.; Corti, A. NGR-tagged nano-gold: A new CD13-selective carrier for cytokine delivery to tumors. Nano Res., 2016, 9(5), 1393-1408.
[http://dx.doi.org/10.1007/s12274-016-1035-8] [PMID: 27226823]
[58]
Guan, Y.Y.; Luan, X.; Xu, J.R.; Liu, Y.R.; Lu, Q.; Wang, C.; Liu, H.J.; Gao, Y.G.; Chen, H.Z.; Fang, C. Selective eradication of tumor vascular pericytes by peptide conjugated nanoparticles for antiangiogenic therapy of melanoma lung metastasis. Biomaterials, 2014, 35(9), 3060-3070.
[http://dx.doi.org/10.1016/j.biomaterials.2013.12.027] [PMID: 24393268]
[59]
Liu, Y.R.; Guan, Y.Y.; Luan, X.; Lu, Q.; Wang, C.; Liu, H.J.; Gao, Y.G.; Yang, S.C.; Dong, X.; Chen, H.Z.; Fang, C. Delta-like ligand 4-targeted nanomedicine for antiangiogenic cancer therapy. Biomaterials, 2015, 42, 161-171.
[http://dx.doi.org/10.1016/j.biomaterials.2014.11.039] [PMID: 25542804]
[60]
Gerosa, F.; Baldani-Guerra, B.; Nisii, C.; Marchesini, V.; Carra, G.; Trinchieri, G. Reciprocal activating interaction between natural killer cells and dendritic cells. J. Exp. Med., 2002, 195(3), 327-333.
[http://dx.doi.org/10.1084/jem.20010938] [PMID: 11828007]
[61]
Keller, C.W.; Freigang, S.; Lünemann, J.D. Reciprocal Crosstalk between Dendritic Cells and Natural Killer T Cells: Mechanisms and Therapeutic Potential. Front. Immunol., 2017, 8, 570.
[http://dx.doi.org/10.3389/fimmu.2017.00570] [PMID: 28596767]
[62]
Mahmood, S.; Upreti, D.; Sow, I.; Amari, A.; Nandagopal, S.; Kung, S.K. Bidirectional interactions of NK cells and dendritic cells in immunotherapy: current and future perspective. Immunotherapy, 2015, 7(3), 301-308.
[http://dx.doi.org/10.2217/imt.14.122] [PMID: 25804481]
[63]
Karimi, K.; Karimi, Y.; Chan, J.; Boudreau, J.E.; Basset, J.; Chew, M.V.; Reid, S.; Bramson, J.L.; Wan, Y.; Ashkar, A.A.; Type, I. Type I IFN signaling on dendritic cells is required for NK cell-mediated anti-tumor immunity. Innate Immun., 2015, 21(6), 626-634.
[http://dx.doi.org/10.1177/1753425915575078] [PMID: 25749844]
[64]
Langers, I.; Renoux, V.; Reschner, A.; Touzé, A.; Coursaget, P.; Boniver, J.; Koch, J.; Delvenne, P.; Jacobs, N. Natural killer and dendritic cells collaborate in the immune response induced by the vaccine against uterine cervical cancer. Eur. J. Immunol., 2014, 44(12), 3585-3595.
[http://dx.doi.org/10.1002/eji.201444594] [PMID: 25229656]
[65]
Barreira da Silva, R.; Graf, C.; Münz, C. Cytoskeletal stabilization of inhibitory interactions in immunologic synapses of mature human dendritic cells with natural killer cells. Blood, 2011, 118(25), 6487-6498.
[http://dx.doi.org/10.1182/blood-2011-07-366328] [PMID: 21917751]
[66]
Morandi, B.; Mortara, L.; Carrega, P.; Cantoni, C.; Costa, G.; Accolla, R.S.; Mingari, M.C.; Ferrini, S.; Moretta, L.; Ferlazzo, G. NK cells provide helper signal for CD8+ T cells by inducing the expression of membrane-bound IL-15 on DCs. Int. Immunol., 2009, 21(5), 599-606.
[http://dx.doi.org/10.1093/intimm/dxp029] [PMID: 19325034]
[67]
Fernandez, N.C.; Lozier, A.; Flament, C.; Ricciardi-Castagnoli, P.; Bellet, D.; Suter, M.; Perricaudet, M.; Tursz, T.; Maraskovsky, E.; Zitvogel, L. Dendritic cells directly trigger NK cell functions: cross talk relevant in innate anti-tumor immune responses in vivo. Nat. Med., 1999, 5(4), 405-411.
[http://dx.doi.org/10.1038/7403] [PMID: 10202929]
[68]
Degli-Esposti, M.A.; Smyth, M.J. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat. Rev. Immunol., 2005, 5(2), 112-124.
[http://dx.doi.org/10.1038/nri1549] [PMID: 15688039]
[69]
Shimizu, K.; Fujii, S. DC therapy induces long-term NK reactivity to tumors via host DC. Eur. J. Immunol., 2009, 39(2), 457-468.
[http://dx.doi.org/10.1002/eji.200838794] [PMID: 19180466]
[70]
Karimi, K.; Boudreau, J.E.; Fraser, K.; Liu, H.; Delanghe, J.; Gauldie, J.; Xing, Z.; Bramson, J.L.; Wan, Y. Enhanced Antitumor Immunity Elicited by Dendritic Cell Vaccines Is a Result of Their Ability to Engage Both CTL and IFNgamma producing NK Cells. Molecular therapy: the j. of the Amer. Soc. of Gene Ther., 2008, 16(2), 411-418.
[http://dx.doi.org/10.1038/sj.mt.6300347] [PMID: 18059374]
[71]
Morandi, B.; Mortara, L.; Chiossone, L.; Accolla, R.S.; Mingari, M.C.; Moretta, L.; Moretta, A.; Ferlazzo, G. Dendritic cell editing by activated natural killer cells results in a more protective cancer-specific immune response. PLoS One, 2012, 7(6) e39170
[http://dx.doi.org/10.1371/journal.pone.0039170] [PMID: 22723958]
[72]
Jacobs, B.; Ullrich, E. The interaction of NK cells and dendritic cells in the tumor environment: how to enforce NK cell & DC action under immunosuppressive conditions? Curr. Med. Chem., 2012, 19(12), 1771-1779.
[http://dx.doi.org/10.2174/092986712800099857] [PMID: 22414086]
[73]
Spaggiari, G.M.; Carosio, R.; Pende, D.; Marcenaro, S.; Rivera, P.; Zocchi, M.R.; Moretta, L.; Poggi, A. NK cell mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46. Eur. J. Immunol., 2001, 31(6), 1656-1665.
[http://dx.doi.org/10.1002/1521-4141(200106)31:6<1656:AID-IMMU1656>3.0.CO;2-V] [PMID: 11385609]
[74]
Carbone, E.; Terrazzano, G.; Ruggiero, G.; Zanzi, D.; Ottaiano, A.; Manzo, C.; Kärre, K.; Zappacosta, S. Recognition of autologous dendritic cells by human NK cells. Eur. J. Immunol., 1999, 29(12), 4022-4029.
[http://dx.doi.org/10.1002/(SICI)1521-4141(199912)29:12<4022:AID-IMMU4022>3.0.CO;2-O] [PMID: 10602012]
[75]
Wilson, J.L.; Heffler, L.C.; Charo, J.; Scheynius, A.; Bejarano, M.T.; Ljunggren, H.G. Targeting of human dendritic cells by autologous NK cells. J. Immunol., 1999, 163(12), 6365-6370.
[PMID: 10586025]
[76]
Pende, D.; Castriconi, R.; Romagnani, P.; Spaggiari, G.M.; Marcenaro, S.; Dondero, A.; Lazzeri, E.; Lasagni, L.; Martini, S.; Rivera, P.; Capobianco, A.; Moretta, L.; Moretta, A.; Bottino, C. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood, 2006, 107(5), 2030-2036.
[http://dx.doi.org/10.1182/blood-2005-07-2696] [PMID: 16304049]
[77]
Poggi, A.; Carosio, R.; Spaggiari, G.M.; Fortis, C.; Tambussi, G.; Dell’Antonio, G.; Dal Cin, E.; Rubartelli, A.; Zocchi, M.R. NK cell activation by dendritic cells is dependent on LFA-1-mediated induction of calcium-calmodulin kinase II: inhibition by HIV-1 Tat C-terminal domain. J. Immunol., 2002, 168(1), 95-101.
[http://dx.doi.org/10.4049/jimmunol.168.1.95] [PMID: 11751951]
[78]
Nedvetzki, S.; Sowinski, S.; Eagle, R.A.; Harris, J.; Vély, F.; Pende, D.; Trowsdale, J.; Vivier, E.; Gordon, S.; Davis, D.M. Reciprocal regulation of human natural killer cells and macrophages associated with distinct immune synapses. Blood, 2007, 109(9), 3776-3785.
[http://dx.doi.org/10.1182/blood-2006-10-052977] [PMID: 17218381]
[79]
Robinette, M.L.; Colonna, M. Innate lymphoid cells and the MHC. HLA, 2016, 87(1), 5-11.
[http://dx.doi.org/10.1111/tan.12723] [PMID: 26812060]
[80]
Long, E.O.; Kim, H.S.; Liu, D.; Peterson, M.E.; Rajagopalan, S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu. Rev. Immunol., 2013, 31, 227-258.
[http://dx.doi.org/10.1146/annurev-immunol-020711-075005] [PMID: 23516982]
[81]
Piccioli, D.; Sbrana, S.; Melandri, E.; Valiante, N.M. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J. Exp. Med., 2002, 195(3), 335-341.
[http://dx.doi.org/10.1084/jem.20010934] [PMID: 11828008]
[82]
Ferlazzo, G.; Tsang, M.L.; Moretta, L.; Melioli, G.; Steinman, R.M.; Münz, C. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J. Exp. Med., 2002, 195(3), 343-351.
[http://dx.doi.org/10.1084/jem.20011149] [PMID: 11828009]
[83]
Martín-Fontecha, A.; Thomsen, L.L.; Brett, S.; Gerard, C.; Lipp, M.; Lanzavecchia, A.; Sallusto, F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol., 2004, 5(12), 1260-1265.
[http://dx.doi.org/10.1038/ni1138] [PMID: 15531883]
[84]
Bouwer, A.L.; Saunderson, S.C.; Caldwell, F.J.; Damani, T.T.; Pelham, S.J.; Dunn, A.C.; Jack, R.W.; Stoitzner, P.; McLellan, A.D. NK cells are required for dendritic cell-based immunotherapy at the time of tumor challenge. J. Immunol., 2014, 192(5), 2514-2521.
[http://dx.doi.org/10.4049/jimmunol.1202797] [PMID: 24477907]
[85]
Nagasaki, E.; Takahara, A.; Koido, S.; Sagawa, Y.; Aiba, K.; Tajiri, H.; Yagita, H.; Homma, S. Combined treatment with dendritic cells and 5-fluorouracil elicits augmented NK cell-mediated antitumor activity through the tumor necrosis factor-alpha pathway. J. Immunother., 2010, 33(5), 467-474.
[http://dx.doi.org/10.1097/CJI.0b013e3181d36726] [PMID: 20463601]
[86]
Johansson, A.; Hamzah, J.; Payne, C.J.; Ganss, R. Tumor targeted TNFα stabilizes tumor vessels and enhances active immunotherapy. Proc. Natl. Acad. Sci. USA, 2012, 109(20), 7841-7846.
[http://dx.doi.org/10.1073/pnas.1118296109] [PMID: 22547817]
[87]
Kirchhofer, D.; Sakariassen, K.S.; Clozel, M.; Tschopp, T.B.; Hadváry, P.; Nemerson, Y.; Baumgartner, H.R. Relationship between tissue factor expression and deposition of fibrin, platelets, and leukocytes on cultured endothelial cells under venous blood flow conditions. Blood, 1993, 81(8), 2050-2058.
[http://dx.doi.org/10.1182/blood.V81.8.2050.2050] [PMID: 8097120]
[88]
Watanabe, N.; Niitsu, Y.; Umeno, H.; Sone, H.; Neda, H.; Yamauchi, N.; Maeda, M.; Urushizaki, I. Synergistic cytotoxic and antitumor effects of recombinant human tumor necrosis factor and hyperthermia. Cancer Res., 1988, 48(3), 650-653.
[PMID: 3335027]
[89]
Fajardo, L.F.; Kwan, H.H.; Kowalski, J.; Prionas, S.D.; Allison, A.C. Dual role of tumor necrosis factor-alpha in angiogenesis. Am. J. Pathol., 1992, 140(3), 539-544.
[PMID: 1372154]
[90]
Folli, S.; Pèlegrin, A.; Chalandon, Y.; Yao, X.; Buchegger, F.; Lienard, D.; Lejeune, F.; Mach, J.P. Tumor-necrosis factor can enhance radio-antibody uptake in human colon carcinoma xenografts by increasing vascular permeability. Int. J. Cancer, 1993, 53(5), 829-836.
[http://dx.doi.org/10.1002/ijc.2910530521] [PMID: 8449608]
[91]
Kristensen, C.A.; Nozue, M.; Boucher, Y.; Jain, R.K. Reduction of interstitial fluid pressure after TNF-alpha treatment of three human melanoma xenografts. Br. J. Cancer, 1996, 74(4), 533-536.
[http://dx.doi.org/10.1038/bjc.1996.397] [PMID: 8761366]
[92]
Kemeny, N.; Childs, B.; Larchian, W.; Rosado, K.; Kelsen, D. A phase II trial of recombinant tumor necrosis factor in patients with advanced colorectal carcinoma. Cancer, 1990, 66(4), 659-663.
[http://dx.doi.org/10.1002/1097-0142(19900815)66:4<659::AIDCNCR2820660410>3.0.CO;2-2] [PMID: 2386895]
[93]
Lejeune, F.J.; Liénard, D.; Matter, M.; Rüegg, C. Efficiency of recombinant human TNF in human cancer therapy. Cancer Immun., 2006, 6, 6.
[PMID: 16551058]
[94]
Lejeune, F.J.; Rüegg, C.; Liénard, D. Clinical applications of TNF-alpha in cancer. Curr. Opin. Immunol., 1998, 10(5), 573-580.
[http://dx.doi.org/10.1016/S0952-7915(98)80226-4] [PMID: 9794839]
[95]
Seinen, J.M.; Hoekstra, H.J. Isolated limb perfusion of soft tissue sarcomas: a comprehensive review of literature. Cancer Treat. Rev., 2013, 39(6), 569-577.
[http://dx.doi.org/10.1016/j.ctrv.2012.10.005] [PMID: 23232098]
[96]
Grünhagen, D.J.; de Wilt, J.H.; ten Hagen, T.L.; Eggermont, A.M. Technology insight: Utility of TNF-alpha-based isolated limb perfusion to avoid amputation of irresectable tumors of the extremities. Nat. Clin. Pract. Oncol., 2006, 3(2), 94-103.
[http://dx.doi.org/10.1038/ncponc0426] [PMID: 16462850]
[97]
Verhoef, C.; de Wilt, J.H.; Grünhagen, D.J.; van Geel, A.N.; ten Hagen, T.L.; Eggermont, A.M. Isolated limb perfusion with melphalan and TNF-alpha in the treatment of extremity sarcoma. Curr. Treat. Options Oncol., 2007, 8(6), 417-427.
[http://dx.doi.org/10.1007/s11864-007-0044-y] [PMID: 18066703]
[98]
Carnemolla, B.; Neri, D.; Castellani, P.; Leprini, A.; Neri, G.; Pini, A.; Winter, G.; Zardi, L. Phage antibodies with pan-species recognition of the oncofoetal angiogenesis marker fibronectin ED-B domain. Int. J. Cancer, 1996, 68(3), 397-405.
[http://dx.doi.org/10.1002/(SICI)1097-0215(19961104)68:3<397::AIDIJC20>3.0.CO;2-4] [PMID: 8903484]
[99]
Villa, A.; Trachsel, E.; Kaspar, M.; Schliemann, C.; Sommavilla, R.; Rybak, J.N.; Rösli, C.; Borsi, L.; Neri, D. A high-affinity human monoclonal antibody specific to the alternatively spliced EDA domain of fibronectin efficiently targets tumor neo-vasculature in vivo. Int. J. Cancer, 2008, 122(11), 2405-2413.
[http://dx.doi.org/10.1002/ijc.23408] [PMID: 18271006]
[100]
Silacci, M.; Brack, S.S.; Späth, N.; Buck, A.; Hillinger, S.; Arni, S.; Weder, W.; Zardi, L.; Neri, D. Human monoclonal antibodies to domain C of tenascin-C selectively target solid tumors in vivo. Protein Eng. Des. Sel., 2006, 19(10), 471-478.
[http://dx.doi.org/10.1093/protein/gzl033] [PMID: 16928692]
[101]
Brack, S.S.; Silacci, M.; Birchler, M.; Neri, D. Tumor-targeting properties of novel antibodies specific to the large isoform of tenascin-C. Clinical cancer research : an official journal of the American Association for Cancer Research, 2006, 12(10), 3200-3208.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-2804]
[102]
Porcellini, S.; Asperti, C.; Valentinis, B.; Tiziano, E.; Mangia, P.; Bordignon, C.; Rizzardi, G.P.; Traversari, C. The tumor vessel targeting agent NGR-TNF controls the different stages of the tumorigenic process in transgenic mice by distinct mechanisms. OncoImmunology, 2015, 4(10) e1041700
[http://dx.doi.org/10.1080/2162402X.2015.1041700] [PMID: 26451306]
[103]
Sacchi, A.; Gasparri, A.; Gallo-Stampino, C.; Toma, S.; Curnis, F.; Corti, A. Synergistic antitumor activity of cisplatin, paclitaxel, and gemcitabine with tumor vasculature-targeted tumor necrosis factor alpha. Clinical cancer research: an official journal of the American Association for Cancer Research,, 2006, 12(1), 175-182.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-1147]
[104]
Ronca, R.; Sozzani, S.; Presta, M.; Alessi, P. Delivering cytokines at tumor site: The immunocytokine-conjugated anti-EDB-fibronectin antibody case. Immunobiology, 2009, 214(9-10), 800-810.
[http://dx.doi.org/10.1016/j.imbio.2009.06.005] [PMID: 19625102]
[105]
van Laarhoven, H.W.; Gambarota, G.; Heerschap, A.; Lok, J.; Verhagen, I.; Corti, A.; Toma, S.; Gallo Stampino, C.; van der Kogel, A.; Punt, C.J. Effects of the tumor vasculature targeting agent NGR-TNF on the tumor microenvironment in murine lymphomas. Invest. New Drugs, 2006, 24(1), 27-36.
[http://dx.doi.org/10.1007/s10637-005-4540-2] [PMID: 16379040]
[106]
Corti, A.; Pastorino, F.; Curnis, F.; Arap, W.; Ponzoni, M.; Pasqualini, R. Targeted drug delivery and penetration into solid tumors. Med. Res. Rev., 2012, 32(5), 1078-1091.
[http://dx.doi.org/10.1002/med.20238] [PMID: 21287572]
[107]
De Bock, K.; Mazzone, M.; Carmeliet, P. Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not? Nat. Rev. Clin. Oncol., 2011, 8(7), 393-404.
[http://dx.doi.org/10.1038/nrclinonc.2011.83] [PMID: 21629216]
[108]
Carmeliet, P.; Jain, R.K. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov., 2011, 10(6), 417-427.
[http://dx.doi.org/10.1038/nrd3455] [PMID: 21629292]
[109]
Goel, S.; Duda, D.G.; Xu, L.; Munn, L.L.; Boucher, Y.; Fukumura, D.; Jain, R.K. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev., 2011, 91(3), 1071-1121.
[http://dx.doi.org/10.1152/physrev.00038.2010] [PMID: 21742796]
[110]
Bottsford-Miller, J.N.; Coleman, R.L.; Sood, A.K. Resistance and escape from antiangiogenesis therapy: clinical implications and future strategies. J. Clin. Oncol., 2012, 30(32), 4026-4034.
[http://dx.doi.org/10.1200/JCO.2012.41.9242] [PMID: 23008289]
[111]
Ebos, J.M.; Kerbel, R.S. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat. Rev. Clin. Oncol., 2011, 8(4), 210-221.
[http://dx.doi.org/10.1038/nrclinonc.2011.21] [PMID: 21364524]
[112]
Joyce, J.A.; Laakkonen, P.; Bernasconi, M.; Bergers, G.; Ruoslahti, E.; Hanahan, D. Stage-specific vascular markers revealed by phage display in a mouse model of pancreatic islet tumorigenesis. Cancer Cell, 2003, 4(5), 393-403.
[http://dx.doi.org/10.1016/S1535-6108(03)00271-X] [PMID: 14667506]
[113]
Johansson, A.; Hamzah, J.; Ganss, R. License for destruction: tumor-specific cytokine targeting. Trends Mol. Med., 2014, 20(1), 16-24.
[http://dx.doi.org/10.1016/j.molmed.2013.10.002] [PMID: 24169116]
[114]
Maniotis, A.J.; Folberg, R.; Hess, A.; Seftor, E.A.; Gardner, L.M.; Pe’er, J.; Trent, J.M.; Meltzer, P.S.; Hendrix, M.J. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol., 1999, 155(3), 739-752.
[http://dx.doi.org/10.1016/S0002-9440(10)65173-5] [PMID: 10487832]
[115]
Fogal, V.; Zhang, L.; Krajewski, S.; Ruoslahti, E. Mitochondrial/cell-surface protein p32/gC1qR as a molecular target in tumor cells and tumor stroma. Cancer Res., 2008, 68(17), 7210-7218.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-6752] [PMID: 18757437]
[116]
Brennen, W.N.; Rosen, D.M.; Wang, H.; Isaacs, J.T.; Denmeade, S.R. Targeting carcinoma-associated fibroblasts within the tumor stroma with a fibroblast activation protein-activated prodrug. J. Natl. Cancer Inst., 2012, 104(17), 1320-1334.
[http://dx.doi.org/10.1093/jnci/djs336] [PMID: 22911669]
[117]
Delgado-Bellido, D.; Serrano-Saenz, S.; Fernández-Cortés, M.; Oliver, F.J. Vasculogenic mimicry signaling revisited: focus on non-vascular VE-cadherin. Mol. Cancer, 2017, 16(1), 65.
[http://dx.doi.org/10.1186/s12943-017-0631-x] [PMID: 28320399]
[118]
Hamzah, J.; Altin, J.G.; Herringson, T.; Parish, C.R.; Hämmerling, G.J.; O’Donoghue, H.; Ganss, R. Targeted liposomal delivery of TLR9 ligands activates spontaneous antitumor immunity in an autochthonous cancer model. J. Immunol., 2009, 183(2), 1091-1098.
[http://dx.doi.org/10.4049/jimmunol.0900736] [PMID: 19561111]
[119]
Kalluri, R. The biology and function of fibroblasts in cancer. Nat. Rev. Cancer, 2016, 16(9), 582-598.
[http://dx.doi.org/10.1038/nrc.2016.73] [PMID: 27550820]
[120]
Poggi, A.; Musso, A.; Dapino, I.; Zocchi, M.R. Mechanisms of tumor escape from immune system: role of mesenchymal stromal cells. Immunol. Lett., 2014, 159(1-2), 55-72.
[http://dx.doi.org/10.1016/j.imlet.2014.03.001] [PMID: 24657523]
[121]
Yang, L. TGFbeta, a potent regulator of tumor microenvironment and host immune response, implication for therapy. Curr. Mol. Med., 2010, 10(4), 374-380.
[http://dx.doi.org/10.2174/156652410791317039] [PMID: 20455854]
[122]
Wang, Z.; Till, B.; Gao, Q. Chemotherapeutic agent-mediated elimination of myeloid derived suppressor cells. OncoImmunology, 2017, 6(7) e1331807
[http://dx.doi.org/10.1080/2162402X.2017.1331807] [PMID: 28811975]
[123]
Kumar, V.; Patel, S.; Tcyganov, E.; Gabrilovich, D.I. The Nature of Myeloid-Derived Suppressor Cells in the Tumor Microenvironment. Trends Immunol., 2016, 37(3), 208-220.
[http://dx.doi.org/10.1016/j.it.2016.01.004] [PMID: 26858199]
[124]
Lu, L.; Barbi, J.; Pan, F. The regulation of immune tolerance by FOXP3. Nat. Rev. Immunol., 2017, 17(11), 703-717.
[http://dx.doi.org/10.1038/nri.2017.75] [PMID: 28757603]
[125]
Dunn, G.P.; Bruce, A.T.; Ikeda, H.; Old, L.J.; Schreiber, R.D. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol., 2002, 3(11), 991-998.
[http://dx.doi.org/10.1038/ni1102-991] [PMID: 12407406]
[126]
Bassani, B.; Baci, D.; Gallazzi, M.; Poggi, A.; Bruno, A.; Mortara, L. Natural Killer Cells as Key Players of Tumor Progression and Angiogenesis: Old and Novel Tools to Divert Their Pro-Tumor Activities into Potent Anti-Tumor Effects. Cancers (Basel), 2019, 11(4), 461.
[http://dx.doi.org/10.3390/cancers11040461] [PMID: 30939820]
[127]
Dredge, K.; Marriott, J.B.; Macdonald, C.D.; Man, H.W.; Chen, R.; Muller, G.W.; Stirling, D.; Dalgleish, A.G. Novel thalidomide analogues display anti-angiogenic activity independently of immunomodulatory effects. Br. J. Cancer, 2002, 87(10), 1166-1172.
[http://dx.doi.org/10.1038/sj.bjc.6600607] [PMID: 12402158]
[128]
Lentzsch, S.; Rogers, M.S.; LeBlanc, R.; Birsner, A.E.; Shah, J.H.; Treston, A.M.; Anderson, K.C.; D’Amato, R.J. S-3-Amino-phthalimido-glutarimide inhibits angiogenesis and growth of B-cell neoplasias in mice. Cancer Res., 2002, 62(8), 2300-2305.
[PMID: 11956087]
[129]
Knight, R. IMiDs: a novel class of immunomodulators. Semin. Oncol., 2005, 32(4)(Suppl. 5), S24-S30.
[http://dx.doi.org/10.1053/j.seminoncol.2005.06.018] [PMID: 16085014]
[130]
Gupta, D.; Treon, S.P.; Shima, Y.; Hideshima, T.; Podar, K.; Tai, Y.T.; Lin, B.; Lentzsch, S.; Davies, F.E.; Chauhan, D.; Schlossman, R.L.; Richardson, P.; Ralph, P.; Wu, L.; Payvandi, F.; Muller, G.; Stirling, D.I.; Anderson, K.C. Adherence of multiple myeloma cells to bone marrow stromal cells upregulates vascular endothelial growth factor secretion: therapeutic applications. Leukemia, 2001, 15(12), 1950-1961.
[http://dx.doi.org/10.1038/sj.leu.2402295] [PMID: 11753617]
[131]
Figg, W.D.; Arlen, P.; Gulley, J.; Fernandez, P.; Noone, M.; Fedenko, K.; Hamilton, M.; Parker, C.; Kruger, E.A.; Pluda, J.; Dahut, W.L. A randomized phase II trial of docetaxel (taxotere) plus thalidomide in androgen-independent prostate cancer. Semin. Oncol., 2001, 28(4)(Suppl. 15), 62-66.
[http://dx.doi.org/10.1016/S0093-7754(01)90157-5] [PMID: 11685731]
[132]
Payvandi, F.; Wu, L.; Naziruddin, S.D.; Haley, M.; Parton, A.; Schafer, P.H.; Chen, R.S.; Muller, G.W.; Hughes, C.C.; Stirling, D.I. Immunomodulatory drugs (IMiDs) increase the production of IL-2 from stimulated T cells by increasing PKC-theta activation and enhancing the DNA-binding activity of AP-1 but not NF-kappaB, OCT-1, or NF-AT. (Journal of interferon and cytokine research : the official journal of the International Society for Interferon and Cytokine Research)2005, 25(10), 604-616.
[http://dx.doi.org/10.1089/jir.2005.25.604]
[133]
Haslett, P.A.; Corral, L.G.; Albert, M.; Kaplan, G. Thalidomide costimulates primary human T lymphocytes, preferentially inducing proliferation, cytokine production, and cytotoxic responses in the CD8+ subset. J. Exp. Med., 1998, 187(11), 1885-1892.
[http://dx.doi.org/10.1084/jem.187.11.1885] [PMID: 9607928]
[134]
LeBlanc, R.; Hideshima, T.; Catley, L.P.; Shringarpure, R.; Burger, R.; Mitsiades, N.; Mitsiades, C.; Cheema, P.; Chauhan, D.; Richardson, P.G.; Anderson, K.C.; Munshi, N.C. Immunomodulatory drug costimulates T cells via the B7-CD28 pathway. Blood, 2004, 103(5), 1787-1790.
[http://dx.doi.org/10.1182/blood-2003-02-0361] [PMID: 14512311]
[135]
Görgün, G.; Calabrese, E.; Soydan, E.; Hideshima, T.; Perrone, G.; Bandi, M.; Cirstea, D.; Santo, L.; Hu, Y.; Tai, Y.T.; Nahar, S.; Mimura, N.; Fabre, C.; Raje, N.; Munshi, N.; Richardson, P.; Anderson, K.C. Immunomodulatory effects of lenalidomide and pomalidomide on interaction of tumor and bone marrow accessory cells in multiple myeloma. Blood, 2010, 116(17), 3227-3237.
[http://dx.doi.org/10.1182/blood-2010-04-279893] [PMID: 20651070]
[136]
Marriott, J.B.; Clarke, I.A.; Dredge, K.; Muller, G.; Stirling, D.; Dalgleish, A.G. Thalidomide and its analogues have distinct and opposing effects on TNF-alpha and TNFR2 during co-stimulation of both CD4(+) and CD8(+) T cells. Clin. Exp. Immunol., 2002, 130(1), 75-84.
[http://dx.doi.org/10.1046/j.1365-2249.2002.01954.x] [PMID: 12296856]
[137]
Corral, L.G.; Haslett, P.A.; Muller, G.W.; Chen, R.; Wong, L.M.; Ocampo, C.J.; Patterson, R.T.; Stirling, D.I.; Kaplan, G. Differential cytokine modulation and T cell activation by two distinct classes of thalidomide analogues that are potent inhibitors of TNF-alpha. J. Immunol., 1999, 163(1), 380-386.
[PMID: 10384139]
[138]
Hayashi, T.; Hideshima, T.; Akiyama, M.; Podar, K.; Yasui, H.; Raje, N.; Kumar, S.; Chauhan, D.; Treon, S.P.; Richardson, P.; Anderson, K.C. Molecular mechanisms whereby immunomodulatory drugs activate natural killer cells: clinical application. Br. J. Haematol., 2005, 128(2), 192-203.
[http://dx.doi.org/10.1111/j.1365-2141.2004.05286.x] [PMID: 15638853]
[139]
Dauguet, N.; Fournié, J.J.; Poupot, R.; Poupot, M. Lenalidomide down regulates the production of interferon-gamma and the expression of inhibitory cytotoxic receptors of human Natural Killer cells. Cell. Immunol., 2010, 264(2), 163-170.
[http://dx.doi.org/10.1016/j.cellimm.2010.06.003] [PMID: 20621290]
[140]
Davies, F.; Baz, R. Lenalidomide mode of action: linking bench and clinical findings. Blood Rev., 2010, 24(Suppl. 1), S13-S19.
[http://dx.doi.org/10.1016/S0268-960X(10)70004-7] [PMID: 21126632]
[141]
Lioznov, M.; El-Cheikh, J., Jr; Hoffmann, F.; Hildebrandt, Y.; Ayuk, F.; Wolschke, C.; Atanackovic, D.; Schilling, G.; Badbaran, A.; Bacher, U.; Fehse, B.; Zander, A.R.; Blaise, D.; Mohty, M.; Kröger, N. Lenalidomide as salvage therapy after allo-SCT for multiple myeloma is effective and leads to an increase of activated NK (NKp44(+)) and T (HLA-DR(+)) cells. Bone Marrow Transplant., 2010, 45(2), 349-353.
[http://dx.doi.org/10.1038/bmt.2009.155] [PMID: 19584825]
[142]
Chamberlain, P.P.; Lopez-Girona, A.; Miller, K.; Carmel, G.; Pagarigan, B.; Chie-Leon, B.; Rychak, E.; Corral, L.G.; Ren, Y.J.; Wang, M.; Riley, M.; Delker, S.L.; Ito, T.; Ando, H.; Mori, T.; Hirano, Y.; Handa, H.; Hakoshima, T.; Daniel, T.O.; Cathers, B.E. Structure of the human Cereblon-DDB1-lenalidomide complex reveals basis for responsiveness to thalidomide analogs. Nat. Struct. Mol. Biol., 2014, 21(9), 803-809.
[http://dx.doi.org/10.1038/nsmb.2874] [PMID: 25108355]
[143]
Hagner, P.R.; Man, H.W.; Fontanillo, C.; Wang, M.; Couto, S.; Breider, M.; Bjorklund, C.; Havens, C.G.; Lu, G.; Rychak, E.; Raymon, H.; Narla, R.K.; Barnes, L.; Khambatta, G.; Chiu, H.; Kosek, J.; Kang, J.; Amantangelo, M.D.; Waldman, M.; Lopez-Girona, A.; Cai, T.; Pourdehnad, M.; Trotter, M.; Daniel, T.O.; Schafer, P.H.; Klippel, A.; Thakurta, A.; Chopra, R.; Gandhi, A.K. CC-122, a pleiotropic pathway modifier, mimics an interferon response and has antitumor activity in DLBCL. Blood, 2015, 126(6), 779-789.
[http://dx.doi.org/10.1182VIA/blood-2015-02-628669] [PMID: 26002965]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 27
ISSUE: 25
Year: 2020
Published on: 22 July, 2020
Page: [4233 - 4248]
Pages: 16
DOI: 10.2174/0929867325666180904121118
Price: $65

Article Metrics

PDF: 26
HTML: 2