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Research Papers

Interleukin-4 receptor-targeted liposomal doxorubicin as a model for enhancing cellular uptake and antitumor efficacy in murine colorectal cancer

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Pages 1641-1650 | Received 16 Mar 2015, Accepted 12 Sep 2015, Published online: 30 Oct 2015

References

  • Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA: Cancer J Clin 2012; 62:10-29; PMID:22237781
  • Pasetto LM, Jirillo A, Iadicicco G, Rossi E, Paris MK, Monfardini S. FOLFOX vs. FOLFIRI: a comparison of regimens in the treatment of colorectal cancer metastases. Anticancer Res 2005; 25:563-76; PMID:15816629
  • Gramont A. Adjuvant therapy of stage II and III colon cancer. Seminars Oncol 2005; 32:11-4; http://dx.doi.org/10.1053/j.seminoncol.2005.06.004
  • Nelms K, Keegan AD, Zamorano J, Ryan JJ, Paul WE. The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 1999; 17:701-38; PMID:10358772; http://dx.doi.org/10.1146/annurev.immunol.17.1.701
  • Kelly-Welch AE, Hanson EM, Boothby MR, Keegan AD. Interleukin-4 and interleukin-13 signaling connections maps. Science 2003; 300:1527-8; PMID:12791978; http://dx.doi.org/10.1126/science.1085458
  • Li BH, Yang XZ, Li PD, Yuan Q, Liu XH, Yuan J, Zhang WJ. IL-4/Stat6 activities correlate with apoptosis and metastasis in colon cancer cells. Biochem Biophys Res Commun 2008; 369:554-60; PMID:18294957; http://dx.doi.org/10.1016/j.bbrc.2008.02.052
  • Li Z, Jiang J, Wang Z, Zhang J, Xiao M, Wang C, Lu Y, Qin Z. Endogenous interleukin-4 promotes tumor development by increasing tumor cell resistance to apoptosis. Cancer Res 2008; 68:8687-94; PMID:18974110; http://dx.doi.org/10.1158/0008-5472.CAN-08-0449
  • DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, Coussens LM. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009; 16:91-102; PMID:19647220; http://dx.doi.org/10.1016/j.ccr.2009.06.018
  • Koller FL, Hwang DG, Dozier EA, Fingleton B. Epithelial interleukin-4 receptor expression promotes colon tumor growth. Carcinogenesis 2010; 31:1010-7; PMID:20176658; http://dx.doi.org/10.1093/carcin/bgq044
  • Ko CW, Cuthbert RJ, Orsi NM, Brooke DA, Perry SL, Markham AF, Coletta PL, Hull MA. Lack of interleukin-4 receptor α chain-dependent signalling promotes azoxymethane-induced colorectal aberrant crypt focus formation in Balb/c mice. J Pathol 2008; 214:603-9; PMID:18220315; http://dx.doi.org/10.1002/path.2316
  • Husain SR, Gill P, Kreitman RJ, Pastan I, Puri RK. Interleukin-4 receptor expression on AIDS-associated Kaposi's sarcoma cells and their targeting by a chimeric protein comprised of circularly permuted interleukin-4 and Pseudomonas exotoxin. Mol Med 1997; 3:327-38; PMID:9205948
  • Obiri NI, Siegel JP, Varricchio F, Puri RK. Expression of high-affinity IL-4 receptors on human melanoma, ovarian and breast carcinoma cells. Clin Exp Immunol 1994; 95:148-55; PMID:8287600; http://dx.doi.org/10.1111/j.1365-2249.1994.tb06029.x
  • Leland P, Taguchi J, Husain SR, Kreitman RJ, Pastan I, Puri RK. Human breast carcinoma cells express type II IL-4 receptors and are sensitive to antitumor activity of a chimeric IL-4-Pseudomonas exotoxin fusion protein in vitro and in vivo. Mol Med 2000; 6:165-78; PMID:10965493
  • Obiri NI, Hillman GG, Haas GP, Sud S, Puri RK. Expression of high affinity interleukin-4 receptors on human renal cell carcinoma cells and inhibition of tumor cell growth in vitro by interleukin-4. J Clin Invest 1993; 91:88-93; PMID:8423237; http://dx.doi.org/10.1172/JCI116205
  • Kioi M, Takahashi S, Kawakami M, Kawakami K, Kreitman RJ, Puri RK. Expression and targeting of interleukin-4 receptor for primary and advanced ovarian cancer therapy. Cancer Res 2005; 65:8388-96; PMID:16166317; http://dx.doi.org/10.1158/0008-5472.CAN-05-1043
  • Puri RK, Leland P, Kreitman RJ, Pastan I. Human neurological cancer cells express interleukin-4 (IL-4) receptors which are targets for the toxic effects of IL4-Pseudomonas exotoxin chimeric protein. Int J Cancer J Int Du Cancer 1994; 58:574-81; http://dx.doi.org/10.1002/ijc.2910580421
  • Kawakami K, Leland P, Puri RK. Structure, function, and targeting of interleukin 4 receptors on human head and neck cancer cells. Cancer Res 2000; 60:2981-7; PMID:10850446
  • Kawakami K, Kawakami M, Puri RK. Overexpressed cell surface interleukin-4 receptor molecules can be successfully targeted for antitumor cytotoxin therapy. Critical Rev Immunol 2001; 21:299-310; http://dx.doi.org/10.1615/CritRevImmunol.v21.i1-3.200
  • Formentini A, Braun P, Fricke H, Link KH, Henne-Bruns D, Kornmann M. Expression of interleukin-4 and interleukin-13 and their receptors in colorectal cancer. Int J Colorectal Dis 2012; 27:1369-76; PMID:22441356; http://dx.doi.org/10.1007/s00384-012-1456-0
  • Kaklamanis L, Gatter KC, Mortensen N, Harris AL. Interleukin-4 receptor and epidermal growth factor receptor expression in colorectal cancer. British J Cancer 1992; 66:712-6; http://dx.doi.org/10.1038/bjc.1992.343
  • Borish LC, Nelson HS, Lanz MJ, Claussen L, Whitmore JB, Agosti JM, Garrison L. Interleukin-4 receptor in moderate atopic asthma. A phase I/II randomized, placebo-controlled trial. Am J Respir Crit Care Med 1999; 160:1816-23; PMID:10588591; http://dx.doi.org/10.1164/ajrccm.160.6.9808146
  • Aversa G, Punnonen J, Cocks BG, de Waal Malefyt R, Vega F, Jr., Zurawski SM, Zurawski G, de Vries JE. An interleukin 4 (IL-4) mutant protein inhibits both IL-4 or IL-13-induced human immunoglobulin G4 (IgG4) and IgE synthesis and B cell proliferation: support for a common component shared by IL-4 and IL-13 receptors. J Exp Med 1993; 178:2213-8; PMID:7504061; http://dx.doi.org/10.1084/jem.178.6.2213
  • Rand RW, Kreitman RJ, Patronas N, Varricchio F, Pastan I, Puri RK. Intratumoral administration of recombinant circularly permuted interleukin-4-Pseudomonas exotoxin in patients with high-grade glioma. Clin Cancer Research 2000; 6:2157-65
  • Kawakami K, Kawakami M, Husain SR, Puri RK. Targeting interleukin-4 receptors for effective pancreatic cancer therapy. Cancer Res 2002; 62:3575-80; PMID:12097255
  • Yang L, Horibe T, Kohno M, Haramoto M, Ohara K, Puri RK, Kawakami K. Targeting interleukin-4 receptor α with hybrid peptide for effective cancer therapy. Mol Cancer Ther 2012; 11:235-43; PMID:22084165; http://dx.doi.org/10.1158/1535-7163.MCT-11-0363
  • Weber F, Asher A, Bucholz R, Berger M, Prados M, Chang S, Bruce J, Hall W, Rainov NG, Westphal M, et al. Safety, tolerability, and tumor response of IL4-Pseudomonas exotoxin (NBI-3001) in patients with recurrent malignant glioma. J Neuro-oncol 2003; 64:125-37
  • Garland L, Gitlitz B, Ebbinghaus S, Pan H, de Haan H, Puri RK, Von Hoff D, Figlin R. Phase I trial of intravenous IL-4 pseudomonas exotoxin protein (NBI-3001) in patients with advanced solid tumors that express the IL-4 receptor. J Immunother 2005; 28:376-81; PMID:16000956; http://dx.doi.org/10.1097/01.cji.0000162782.86008.mL
  • Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science 2004; 303:1818-22; PMID:15031496; http://dx.doi.org/10.1126/science.1095833
  • Song G, Wu H, Yoshino K, Zamboni WC. Factors affecting the pharmacokinetics and pharmacodynamics of liposomal drugs. J Liposome Res 2012; 22:177-92; PMID:22332871; http://dx.doi.org/10.3109/08982104.2012.655285
  • Schwendener RA. Liposomes in biology and medicine. Adv Exp Med Biol 2007; 620:117-28; PMID:18217339; http://dx.doi.org/10.1007/978-0-387-76713-0_9
  • Maurer N, Fenske DB, Cullis PR. Developments in liposomal drug delivery systems. Expert Opin Biol Ther 2001; 1:923-47; PMID:11728226; http://dx.doi.org/10.1517/14712598.1.6.923
  • Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov 2005; 4:145-60; PMID:15688077; http://dx.doi.org/10.1038/nrd1632
  • Allen TM. Liposomes. Opportunities in drug delivery. Drugs 1997; 54 Suppl 4:8-14; PMID:9361956; http://dx.doi.org/10.2165/00003495-199700544-00004
  • Dass CR, Walker TL, Burton MA, Decruz EE. Enhanced anticancer therapy mediated by specialized liposomes. J Pharmacy Pharmacol 1997; 49:972-5; http://dx.doi.org/10.1111/j.2042-7158.1997.tb06025.x
  • Hong HY, Lee HY, Kwak W, Yoo J, Na MH, So IS, Kwon TH, Park HS, Huh S, Oh GT, et al. Phage display selection of peptides that home to atherosclerotic plaques: IL-4 receptor as a candidate target in atherosclerosis. J Cell Mol Med 2008; 12:2003-14; PMID:19012727; http://dx.doi.org/10.1111/j.1582-4934.2008.00189.x
  • Wu XL, Kim JH, Koo H, Bae SM, Shin H, Kim MS, Lee BH, Park RW, Kim IS, Choi K, et al. Tumor-targeting peptide conjugated pH-responsive micelles as a potential drug carrier for cancer therapy. Bioconjug Chem 2010; 21:208-13; PMID:20073455; http://dx.doi.org/10.1021/bc9005283
  • Kim JH, Bae SM, Na MH, Shin H, Yang YJ, Min KH, Choi KY, Kim K, Park RW, Kwon IC, et al. Facilitated intracellular delivery of peptide-guided nanoparticles in tumor tissues. J Control Release 2012; 157:493-9; PMID:21945679; http://dx.doi.org/10.1016/j.jconrel.2011.09.070
  • Yang FY, Wang HE, Liu RS, Teng MC, Li JJ, Lu M, Wei MC, Wong TT. Pharmacokinetic analysis of 111 in-labeled liposomal Doxorubicin in murine glioblastoma after blood-brain barrier disruption by focused ultrasound. PloS One 2012; 7:e45468; PMID:23029030; http://dx.doi.org/10.1371/journal.pone.0045468
  • Husain SR, Behari N, Kreitman RJ, Pastan I, Puri RK. Complete regression of established human glioblastoma tumor xenograft by interleukin-4 toxin therapy. Cancer Res 1998; 58:3649-53; PMID:9721874
  • Yang FY, Wong TT, Teng MC, Liu RS, Lu M, Liang HF, Wei MC. Focused ultrasound and interleukin-4 receptor-targeted liposomal doxorubicin for enhanced targeted drug delivery and antitumor effect in glioblastoma multiforme. J Control Release 2012; 160:652-8; PMID:22405901; http://dx.doi.org/10.1016/j.jconrel.2012.02.023
  • Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F, Tripodo C, Russo A, Gulotta G, Medema JP, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007; 1:389-402; PMID:18371377; http://dx.doi.org/10.1016/j.stem.2007.08.001
  • Todaro M, Perez Alea M, Scopelliti A, Medema JP, Stassi G. IL-4-mediated drug resistance in colon cancer stem cells. Cell Cycle 2008; 7:309-13; PMID:18235245; http://dx.doi.org/10.4161/cc.7.3.5389
  • Francipane MG, Alea MP, Lombardo Y, Todaro M, Medema JP, Stassi G. Crucial role of interleukin-4 in the survival of colon cancer stem cells. Cancer Res 2008; 68:4022-5; PMID:18519657; http://dx.doi.org/10.1158/0008-5472.CAN-07-6874
  • Di Stefano AB, Iovino F, Lombardo Y, Eterno V, Hoger T, Dieli F, Stassi G, Todaro M. Survivin is regulated by interleukin-4 in colon cancer stem cells. J Cell Physiol 2010; 225:555-61; PMID:20506498; http://dx.doi.org/10.1002/jcp.22238
  • The ClinicalTrials. gov website. Intravenous Interleukin-4 PE38KDEL cytotoxin in treating patients with recurrent or metastatic kidney cancer, non-small cell lung cancer, or breast cancer. Available: http://clinicaltrials.gov/ct2/show/NCT00039052?term=IL-4+Receptor&rank=4. Acessed 2013 DEC 10
  • Yang FY, Teng MC, Lu M, Liang HF, Lee YR, Yen CC, Liang ML, Wong TT. Treating glioblastoma multiforme with selective high-dose liposomal doxorubicin chemotherapy induced by repeated focused ultrasound. Int J Nanomedicine 2012; 7:965-74; PMID:22393293; http://dx.doi.org/10.2147/IJN.S29229
  • Shimamura T, Royal RE, Kioi M, Nakajima A, Husain SR, Puri RK. Interleukin-4 cytotoxin therapy synergizes with gemcitabine in a mouse model of pancreatic ductal adenocarcinoma. Cancer Res 2007; 67:9903-12; PMID:17942922; http://dx.doi.org/10.1158/0008-5472.CAN-06-4558
  • Kawakami M, Kawakami K, Kioi M, Leland P, Puri RK. Hodgkin lymphoma therapy with interleukin-4 receptor-directed cytotoxin in an infiltrating animal model. Blood 2005; 105:3707-13; PMID:15626735; http://dx.doi.org/10.1182/blood-2004-08-3216
  • Davis ME, Chen ZG, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 2008; 7:771-82; PMID:18758474; http://dx.doi.org/10.1038/nrd2614
  • Rahman AM, Yusuf SW, Ewer MS. Anthracycline-induced cardiotoxicity and the cardiac-sparing effect of liposomal formulation. Int J Nanomedicine 2007; 2:567-83; PMID:18203425
  • Batist G. Cardiac safety of liposomal anthracyclines. Cardiovasc Toxicol 2007; 7:72-4; PMID:17652807; http://dx.doi.org/10.1007/s12012-007-0014-4
  • Sarangthem V, Cho EA, Bae SM, Singh TD, Kim SJ, Kim S, Jeon WB, Lee BH, Park RW. Construction and application of elastin like polypeptide containing IL-4 receptor targeting peptide. PloS One 2013; 8:e81891; PMID:24339977; http://dx.doi.org/10.1371/journal.pone.0081891
  • Danhier F, Feron O, Preat V. To exploit the tumor microenvironment: Passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J Control Release 2010; 148:135-46; PMID:20797419; http://dx.doi.org/10.1016/j.jconrel.2010.08.027
  • Chua YJ, Cunningham D. Recent data with anti-epidermal growth factor receptor antibodies and irinotecan in colon cancer. Clin Colorectal Cancer 2005; 5 Suppl 2:S81-8; PMID:16336753; http://dx.doi.org/10.3816/CCC.2005.s.011
  • Wang WS, Chen PM, Su Y. Colorectal carcinoma: from tumorigenesis to treatment. Cell Mol Life Sci 2006; 63:663-71; PMID:16501890; http://dx.doi.org/10.1007/s00018-005-5425-4
  • Stacy AE, Jansson PJ, Richardson DR. Molecular pharmacology of ABCG2 and its role in chemoresistance. Mol Pharmacol 2013; 84:655-69; PMID:24021215; http://dx.doi.org/10.1124/mol.113.088609
  • Wang J, Goh B, Lu W, Zhang Q, Chang A, Liu XY, Tan TM, Lee H. In vitro cytotoxicity of Stealth liposomes co-encapsulating doxorubicin and verapamil on doxorubicin-resistant tumor cells. Biol Pharmaceutical Bulletin 2005; 28:822-8; http://dx.doi.org/10.1248/bpb.28.822
  • Li B, Xu H, Li Z, Yao M, Xie M, Shen H, Shen S, Wang X, Jin Y. Bypassing multidrug resistance in human breast cancer cells with lipid/polymer particle assemblies. Int J Nanomedicine 2012; 7:187-97; PMID:22275834
  • Li X, Ding L, Xu Y, Wang Y, Ping Q. Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int Pharmaceutics 2009; 373:116-23; http://dx.doi.org/10.1016/j.ijpharm.2009.01.023
  • Paster W, Bruger AM, Katsch K, Gregoire C, Roncagalli R, Fu G, Gascoigne NR, Nika K, Cohnen A, Feller SM, et al. A THEMIS:SHP1 complex promotes T-cell survival. EMBO J 2015; 34:393-409; PMID:25535246; http://dx.doi.org/10.15252/embj.201387725

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