Inhibition of tumor growth and metastasis by EMMPRIN multiple antigenic peptide (MAP) vaccination is mediated by immune modulation

References

• Melief CJM, van Hall T, Arens R, Ossendorp F, van der Burg SH. Therapeutic cancer vaccines. J Clin Invest 2015; 125:3401-12; PMID:26214521; http://dx.doi.org/10.1172/JCI80009
   PubMed Web of Science ®Google Scholar
• Iero M, Filipazzi P, Castelli C, Belli F, Valdagni R, Parmiani G, Patuzzo R, Santinami M, Rivoltini L. Modified peptides in anti-cancer vaccines: Are we eventually improving anti-tumour immunity? Cancer Immunol Immunother 2009; 58:1159-67; PMID:18998128; http://dx.doi.org/10.1007/s00262-008-0610-6
   PubMed Web of Science ®Google Scholar
• Jensen SM, Twitty CG, Maston LD, Antony PA, Lim M, Hu H-M, Petrausch U, Restifo NP, Fox BA. Increased frequency of suppressive regulatory T cells and T cell-mediated antigen loss results in murine melanoma recurrence. J Immunol 2012; 189:767-76; PMID:22723522; http://dx.doi.org/10.4049/jimmunol.1103822
   PubMed Web of Science ®Google Scholar
• Olson BM, McNeel DG. Antigen loss and tumor-mediated immunosuppression facilitate tumor recurrence. Expert Rev Vaccines 2012; 11:1315-7; PMID:23249231; http://dx.doi.org/10.1586/erv.12.107
   PubMed Web of Science ®Google Scholar
• Pedersen SR, Sørensen MR, Buus S, Christensen JP, Thomsen AR. Comparison of vaccine-induced effector CD8 T cell responses directed against self- and non-self-tumor antigens: implications for cancer immunotherapy. J Immunol 2013; 191:3955-67; PMID:24018273; http://dx.doi.org/10.4049/jimmunol.1300555
   PubMed Web of Science ®Google Scholar
• Gajewski TF, Schreiber H, Fu Y-X. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013; 14:1014-22; PMID:24048123; http://dx.doi.org/10.1038/ni.2703
   PubMed Web of Science ®Google Scholar
• Kissick HT, Sanda MG. The role of active vaccination in cancer immunotherapy: lessons from clinical trials. Curr Opin Immunol 2015; 35:15-22; PMID:26050634; http://dx.doi.org/10.1016/j.coi.2015.05.004
   PubMed Web of Science ®Google Scholar
• Ilyas S, Yang JC. Landscape of Tumor Antigens in T Cell Immunotherapy. J Immunol 2015; 195:5117-22; PMID:26589749; http://dx.doi.org/10.4049/jimmunol.1501657
   PubMed Web of Science ®Google Scholar
• Pol J, Bloy N, Buqué A, Eggermont A, Cremer I, Sautès-Fridman C, Galon J, Tartour E, Zitvogel L, Kroemer G et al. Trial Watch: Peptide-based anticancer vaccines. Oncoimmunology 2015; 4:e974411; PMID:26137405; http://dx.doi.org/10.4161/2162402X.2014.974411
   PubMed Web of Science ®Google Scholar
• Harao M, Mittendorf EA, Radvanyi LG. Peptide-based vaccination and induction of CD8+ T-cell responses against tumor antigens in breast cancer. BioDrugs 2015; 29:15-30; PMID:25523015; http://dx.doi.org/10.1007/s40259-014-0114-1
   PubMed Web of Science ®Google Scholar
• Tam JP. Synthetic peptide vaccine design: synthesis and properties of a high-density multiple antigenic peptide system. Proc Natl Acad Sci USA 1988; 85:5409-13; PMID:3399498; http://dx.doi.org/10.1073/pnas.85.15.5409
   PubMed Web of Science ®Google Scholar
• Bracci L, Falciani C, Lelli B, Lozzi L, Runci Y, Pini A, De Montis MG, Tagliamonte A, Neri P. Synthetic peptides in the form of dendrimers become resistant to protease activity. J Biol Chem 2003; 278:46590-5; PMID:12972419; http://dx.doi.org/10.1074/jbc.M308615200
   PubMed Web of Science ®Google Scholar
• Falciani C, Lozzi L, Pini A, Corti F, Fabbrini M, Bernini A, Lelli B, Niccolai N, Bracci L. Molecular basis of branched peptides resistance to enzyme proteolysis. Chem Biol Drug Des 2007; 69:216-21; PMID:17441908; http://dx.doi.org/10.1111/j.1747-0285.2007.00487.x
   PubMed Web of Science ®Google Scholar
• Ciesielski MJ, Kazim AL, Barth RF, Fenstermaker RA. Cellular antitumor immune response to a branched lysine multiple antigenic peptide containing epitopes of a common tumor-specific antigen in a rat glioma model. Cancer Immunol Immunother 2005; 54:107-19; PMID:15340764; http://dx.doi.org/10.1007/s00262-004-0576-y
   PubMed Web of Science ®Google Scholar
• Zhang J, Yang J, Han X, Zhao Z, Du L, Yu T, Wang H. Overexpression of heparanase multiple antigenic peptide 2 is associated with poor prognosis in gastric cancer: Potential for therapy. Oncol Lett 2012; 4:178-82; PMID:22807984; http://dx.doi.org/10.3892/ol.2012.703
   PubMed Web of Science ®Google Scholar
• Tang X-D, Wang G-Z, Guo J, Lu M-H, Li C, Li N, Chao Y-L, Li C-Z, Wu Y-Y, Hu C-J et al. Multiple antigenic peptides based on H-2Kb-restricted CTL epitopes from murine heparanase induce a potent antitumor immune response in vivo. Mol Cancer Ther 2012; 11:1183-92; PMID:22442309; http://dx.doi.org/10.1158/1535-7163.MCT-11-0607
   PubMed Web of Science ®Google Scholar
• Bai Y, Huang W, Ma L-T, Jiang J-L, Chen Z-N. Importance of N-glycosylation on CD147 for its biological functions. Int J Mol Sci 2014; 15:6356-77; PMID:24739808; http://dx.doi.org/10.3390/ijms15046356
   PubMed Web of Science ®Google Scholar
• Weidle UH, Scheuer W, Eggle D, Klostermann S, Stockinger H. Cancer-related issues of CD147. Cancer Genomics Proteomics 2010; 7:157-69; PMID:20551248
   PubMedGoogle Scholar
• Kanekura T, Chen X. CD147/basigin promotes progression of malignant melanoma and other cancers. J Dermatol Sci 2010; 57:149-54; PMID:20060267; http://dx.doi.org/10.1016/j.jdermsci.2009.12.008
   PubMed Web of Science ®Google Scholar
• Voigt H, Vetter-Kauczok CS, Schrama D, Hofmann UB, Becker JC, Houben R. CD147 impacts angiogenesis and metastasis formation. Cancer Invest 2009; 27:329-33; PMID:19160100; http://dx.doi.org/10.1080/07357900802392675
   PubMed Web of Science ®Google Scholar
• Zhou J, Zhu P, Jiang JL, Zhang Q, Wu ZB, Yao XY, Tang H, Lu N, Yang Y, Chen ZN. Involvement of CD147 in overexpression of MMP-2 and MMP-9 and enhancement of invasive potential of PMA-differentiated THP-1. BMC Cell Biol 2005; 6:25; PMID:15904490; http://dx.doi.org/10.1186/1471-2121-6-25
   PubMed Web of Science ®Google Scholar
• Bougatef F, Quemener C, Kellouche S, Naïmi B, Podgorniak MP, Millot G, Gabison EE, Calvo F, Dosquet C, Lebbé C et al. EMMPRIN promotes angiogenesis through hypoxia-inducible factor-2α-mediated regulation of soluble VEGF isoforms and their receptor VEGFR-2. Blood 2009; 114:5547-56; PMID:19837976; http://dx.doi.org/10.1182/blood-2009-04-217380
   PubMed Web of Science ®Google Scholar
• Zhu X, Song Z, Zhang S, Nanda A, Li G. CD147: a novel modulator of inflammatory and immune disorders. Curr Med Chem 2014; 21:2138-45; PMID:24372217; http://dx.doi.org/10.2174/0929867321666131227163352
   PubMed Web of Science ®Google Scholar
• Yurchenko V, Constant S, Eisenmesser E, Bukrinsky M. Cyclophilin-CD147 interactions: a new target for anti-inflammatory therapeutics. Clin Exp Immunol 2010; 160:305-17; PMID:20345978; http://dx.doi.org/10.1111/j.1365-2249.2010.04115.x
   PubMed Web of Science ®Google Scholar
• Walter M, Simanovich E, Brod V, Lahat N, Bitterman H, Rahat MA. An epitope-specific novel anti-EMMPRIN polyclonal antibody inhibits tumor progression. Oncoimmunology 2015; 5:e1078056; PMID:27057452; http://dx.doi.org/10.1080/2162402X.2015.1078056
   PubMedGoogle Scholar
• Saxena M, Christofori G. Rebuilding cancer metastasis in the mouse. Mol Oncol 2013; 7:283-96; PMID:23474222; http://dx.doi.org/10.1016/j.molonc.2013.02.009
   PubMed Web of Science ®Google Scholar
• Perske C, Lahat N, Sheffy Levin S, Bitterman H, Hemmerlein B, Rahat MA. Loss of inducible nitric oxide synthase expression in the mouse renal cell carcinoma cell line RENCA is mediated by microRNA miR-146a. Am J Pathol 2010; 177:2046-54; PMID:20709800; http://dx.doi.org/10.2353/ajpath.2010.091111
   PubMed Web of Science ®Google Scholar
• Brandacher G, Winkler C, Schroecksnadel K, Margreiter R, Fuchs D. Antitumoral activity of interferon-gamma involved in impaired immune function in cancer patients. Curr Drug Metab 2006; 7:599-612; PMID:16918315; http://dx.doi.org/10.2174/138920006778017768
   PubMed Web of Science ®Google Scholar
• Falciani C, Pini A, Bracci L. Oligo-branched peptides for tumor targeting: from magic bullets to magic forks. Expert Opin Biol Ther 2009; 9:171-8; PMID:19236247; http://dx.doi.org/10.1517/14712590802620501
   PubMed Web of Science ®Google Scholar
• Wang GZ, Tang XD, Lü MH, Gao JH, Liang GP, Li N, Li CZ, Wu YY, Chen L, Cao YL et al. Multiple antigenic peptides of human heparanase elicit a much more potent immune response against tumors. Cancer Prev Res 2011; 4:1285-95; http://dx.doi.org/10.1158/1940-6207.CAPR-11-0083
   PubMed Web of Science ®Google Scholar
• Liao ZL, Tang XD, Lü MH, Wu YY, Cao YL, Fang DC, Yang SM, Guo H. Antitumor effect of new multiple antigen peptide based on HLA-A0201-restricted CTL epitopes of human telomerase reverse transcriptase (hTERT). Cancer Sci 2012; 103:1920-8; PMID:22909416; http://dx.doi.org/10.1111/j.1349-7006.2012.02410.x
   PubMed Web of Science ®Google Scholar
• Zuniga RM, Torcuator R, Jain R, Anderson J, Doyle T, Schultz L, Mikkelsen T. Rebound tumour progression after the cessation of bevacizumab therapy in patients with recurrent high-grade glioma. J Neurooncol 2010; 99:237-42; PMID:20151176; http://dx.doi.org/10.1007/s11060-010-0121-0
   PubMed Web of Science ®Google Scholar
• Ulloa-Montoya F, Louahed J, Dizier B, Gruselle O, Spiessens B, Lehmann FF, Suciu S, Kruit WHJ, Eggermont AMM, Vansteenkiste J et al. Predictive gene signature in MAGE-A3 antigen-specific cancer immunotherapy. J Clin Oncol 2013; 31:2388-95; PMID:23715562; http://dx.doi.org/10.1200/JCO.2012.44.3762
   PubMed Web of Science ®Google Scholar
• Wang E, Bedognetti D, Marincola FM. Prediction of response to anticancer immunotherapy using gene signatures. J Clin Oncol 2013; 31:2369-71; PMID:23715576; http://dx.doi.org/10.1200/JCO.2013.49.2157
   PubMed Web of Science ®Google Scholar
• Zaidi MR, Merlino G. The two faces of interferon-gamma in cancer. Clin Cancer Res 2011; 17:6118-24; PMID:21705455; http://dx.doi.org/10.1158/1078-0432.CCR-11-0482
   PubMed Web of Science ®Google Scholar
• Pini A, Falciani C, Mantengoli E, Bindi S, Brunetti J, Iozzi S, Rossolini GM, Bracci L. A novel tetrabranched antimicrobial peptide that neutralizes bacterial lipopolysaccharide and prevents septic shock in vivo. FASEB J 2010; 24:1015-22; PMID:19917670; http://dx.doi.org/10.1096/fj.09-145474
   PubMed Web of Science ®Google Scholar
• Wang XY, Huang ZX, Chen YG, Lu X, Zhu P, Wen K, Fu N, Liu BY. A multiple antigenic peptide mimicking peptidoglycan induced T cell responses to protect mice from systemic infection with Staphylococcus aureus. PLoS One 2015; 10:1-17; PMID:26317210; http://dx.doi.org/10.1371/journal.pone.0136888
   Web of Science ®Google Scholar
• Zhang J, Yang J, Cai Y, Jin N, Wang H, Yu T. Multiple antigenic polypeptide composed of heparanase B-cell epitopes shrinks human hepatocellular carcinoma in mice. Oncol Rep 2015; 33:1248-56; PMID:25522727; http://dx.doi.org/10.3892/or.2014.3679
   PubMed Web of Science ®Google Scholar
• Kennedy R, Celis E. Multiple roles for CD4+ T cells in anti-tumor immune responses. Immunol Rev 2008; 222:129-44; PMID:18363998; http://dx.doi.org/10.1111/j.1600-065X.2008.00616.x
   PubMed Web of Science ®Google Scholar
• Xiong L, Edwards CK, Zhou L. The biological function and clinical utilization of CD147 in human diseases: a review of the current scientific literature. Int J Mol Sci 2014; 15:17411-41; PMID:25268615; http://dx.doi.org/10.3390/ijms151017411
   PubMed Web of Science ®Google Scholar
• Grass GD, Toole BP. How, with whom and when: an overview of CD147-mediated regulatory networks influencing matrix metalloproteinase activity. Biosci Rep 2016; 36:e00283; http://dx.doi.org/10.1042/BSR20150256
   Google Scholar
• Weibel ER, Kistler GS, Scherle WF. Practical stereological methods for morphometric cytology. J Cell Biol 1966; 30:23-38; PMID:5338131; http://dx.doi.org/10.1083/jcb.30.1.23
   PubMed Web of Science ®Google Scholar
• Almeida JS, Iriabho EE, Gorrepati VL, Wilkinson SR, Grüneberg A, Robbins DE, Hackney JR. ImageJS: Personalized, participated, pervasive, and reproducible image bioinformatics in the web browser. J Pathol Inform 2012; 3:25; PMID:22934238; http://dx.doi.org/10.4103/2153-3539.98813
   PubMedGoogle Scholar