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original research

Therapeutic efficacy of combined vaccination against tumor pericyte-associated antigens DLK1 and DLK2 in mice

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Article: e1290035 | Received 17 Nov 2016, Accepted 26 Jan 2017, Published online: 30 Mar 2017

References

  • Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285(21):1182-6; PMID:4938153; http://dx.doi.org/10.1056/NEJM197111182852108
  • Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, Jain RK. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 2011;91(3):1071-121; PMID: 21742796; http://dx.doi.org/10.1152/physrev.00038.2010
  • Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 2007;6(4):273-86; PMID: 17396134; http://dx.doi.org/10.1038/nrd2115
  • Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008;8(8):592-603; PMID:18650835; http://dx.doi.org/10.1038/nrc2442
  • Bergers G and S Song The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 2005;7(4):452-64; PMID:16212810; http://dx.doi.org/10.1215/S1152851705000232
  • Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, McDonald DM. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 2002;160(3):985-1000; PMID:11891196; http://dx.doi.org/10.1016/S0002-9440(10)64920-6
  • Ghilardi C, Chiorino G, Dossi R, Nagy Z, Giavazzi R, Bani M. Identification of novel vascular markers through gene expression profiling of tumor-derived endothelium. BMC Genomics 2008;9:201; PMID:18447899; http://dx.doi.org/10.1186/1471-2164-9-201
  • Hofmeister V, Schrama D, Becker JC. Anti-cancer therapies targeting the tumor stroma. Cancer Immunol Immunother 2008;57(1):1-17; PMID:17661033; http://dx.doi.org/10.1007/s00262-007-0365-5
  • Zhao X, Bose A, Komita H, Taylor JL, Chi N, Lowe DB, Okada H, Cao Y, Mukhopadhyay D, Cohen PA et al. Vaccines targeting tumor blood vessel antigens promote CD8(+) T cell-dependent tumor eradication or dormancy in HLA-A2 transgenic mice. J Immunol 2012;188(4):1782-8; PMID:22246626; http://dx.doi.org/10.4049/jimmunol.1101644
  • Chi Sabins N, Taylor JL, Fabian KP, Appleman LJ, Maranchie JK, Stolz DB, Storkus WJ. DLK1: a novel target for immunotherapeutic remodeling of the tumor blood vasculature. Mol Ther 2013;21(10):1958-68; PMID:23896726; http://dx.doi.org/10.1038/mt.2013.133
  • Espina AG, Méndez-Vidal C, Moreno-Mateos MA, Sáez C, Romero-Franco A, Japón MA, Pintor-Toro JA. Induction of Dlk1 by PTTG1 inhibits adipocyte differentiation and correlates with malignant transformation. Mol Biol Cell 2009;20(14):3353-62; PMID: 19477929; http://dx.doi.org/10.1091/mbc.E08-09-0965
  • Begum A, Kim Y, Lin Q, Yun Z. DLK1, delta-like 1 homolog (Drosophila), regulates tumor cell differentiation in vivo. Cancer letters 2012;318(1):26-33; PMID: 22142700; http://dx.doi.org/10.1016/j.canlet.2011.11.032
  • Kim Y, Lin Q, Zelterman D, Yun Z. Hypoxia-regulated delta-like 1 homologue enhances cancer cell stemness and tumorigenicity. Cancer research 2009;69(24):9271-80; PMID:19934310; http://dx.doi.org/10.1158/0008-5472.CAN-09-1605
  • Xu X, Liu RF, Zhang X, Huang LY, Chen F, Fei QL, Han ZG. DLK1 as a potential target against cancer stem/progenitor cells of hepatocellular carcinoma. Mol Cancer Ther 2012;11(3):629-38; PMID:22238367; http://dx.doi.org/10.1158/1535-7163.MCT-11-0531
  • Smas CM, Sul HS. Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation. Cell 1993;73(4):725-734; PMID:8500166; http://dx.doi.org/10.1016/0092-8674(93)90252-L
  • Nueda ML, Baladrón V, García-Ramírez JJ, Sánchez-Solana B, Ruvira MD, Rivero S, Ballesteros MA, Monsalve EM, Díaz-Guerra MJ, Ruiz-Hidalgo MJ et al. The novel gene EGFL9/Dlk2, highly homologous to Dlk1, functions as a modulator of adipogenesis. J Mol Biol 2007;367(5):1270-80; PMID:17320102; http://dx.doi.org/10.1016/j.jmb.2006.10.020
  • Sanchez-Solana B, Nueda ML, Ruvira MD, Ruiz-Hidalgo MJ, Monsalve EM, Rivero S, García-Ramírez JJ, Díaz-Guerra MJ, Baladrón V, Laborda J. The EGF-like proteins DLK1 and DLK2 function as inhibitory non-canonical ligands of NOTCH1 receptor that modulate each other's activities. Biochim Biophys Acta 2011;1813(6);1153-64; PMID:21419176; http://dx.doi.org/10.1016/j.bbamcr.2011.03.004
  • Baladron V, Ruiz-Hidalgo MJ, Nueda ML, Díaz-Guerra MJ, García-Ramírez JJ, Bonvini E, Gubina E, Laborda J. dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats. Exp Cell Res 2005;303(2):343-59; PMID:15652348; http://dx.doi.org/10.1016/j.yexcr.2004.10.001
  • Traustadóttir GÁ, Jensen CH, Thomassen M, Beck HC, Mortensen SB, Laborda J, Baladrón V, Sheikh SP, Andersen DC. Evidence of non-canonical NOTCH signaling: Delta-like 1 homolog (DLK1) directly interacts with the NOTCH1 receptor in mammals. Cellular Signalling 2016;28(4):246-254; PMID:26791579; http://dx.doi.org/10.1016/j.cellsig.2016.01.003
  • Sainson RCA, Harris AL. Regulation of angiogenesis by homotypic and heterotypic notch signalling in endothelial cells and pericytes: from basic research to potential therapies. Angiogenesis 2008;11(1):41-51; http://dx.doi.org/10.1007/s10456-008-9098-0
  • He Y, Zhang J, Donahue C, Falo LD Jr. Skin-derived dendritic cells induce potent CD8(+) T cell immunity in recombinant lentivector-mediated genetic immunization. Immunity 2006;24(5):643-56; PMID:16713981; http://dx.doi.org/10.1016/j.immuni.2006.03.014
  • Wentink MQ, Huijbers EJ, De Gruijl TD, Verheul HM, Olsson AK, Griffioen AW. Vaccination approach to anti-angiogenic treatment of cancer. Biochim Biophys Acta 2015;1855(2):155-171; PMID:25641676; http://dx.doi.org/10.1016/j.bbcan.2015.01.005
  • Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis — correlation in invasive breast carcinoma. N Engl J Med 1991;324(1):1-8; PMID:1701519; http://dx.doi.org/10.1056/NEJM199101033240101
  • Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307(5706):58-62; PMID:15637262; http://dx.doi.org/10.1126/science.1104819
  • Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol 2005;25(13):5675-86; PMID:15964822; http://dx.doi.org/10.1128/MCB.25.13.5675-5686.2005
  • Dengler VL, Galbraith M. Espinosa Jí, Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol 2014;49(1):1-15; PMID: 24099156; http://dx.doi.org/10.3109/10409238.2013.838205
  • Bertout JA, Majmundar AJ, Gordan JD, Lam JC, Ditsworth D, Keith B, Brown EJ, Nathanson KL, Simon MC. HIF2α inhibition promotes p53 pathway activity, tumor cell death, and radiation responses. Proc Natl Acad Sci USA 2009;106(34):14391-6; PMID:19706526; http://dx.doi.org/10.1073/pnas.0907357106
  • Kumar V, Gabrilovich DI. Hypoxia-inducible factors in regulation of immune responses in tumour microenvironment. Immunology 2014;143(4):512-9; PMID:25196648; http://dx.doi.org/10.1111/imm.12380
  • Van der Burg SH, Arens R, Ossendorp F, Van Hall T, Melief CJ. Vaccines for established cancer: overcoming the challenges posed by immune evasion. Nat Rev Cancer 2016;16(4):219-233; PMID: 26965076; http://dx.doi.org/10.1038/nrc.2016.16
  • Melief CJ, van Hall T, Arens R, Ossendorp F, van der Burg SH. Therapeutic cancer vaccines. J Clin Invest 2015;125(9):3401-12; PMID:26214521; http://dx.doi.org/10.1172/JCI80009
  • Abiko K, Matsumura N, Hamanishi J, Horikawa N, Murakami R, Yamaguchi K, Yoshioka Y, Baba T, Konishi I, Mandai M. IFN-γ from lymphocytes induces PD-L1 expression and promotes progression of ovarian cancer. Br J Cancer 2015;112(9):1501-9; PMID:25867264; http://dx.doi.org/10.1038/bjc.2015.101
  • Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, Garkavtsev I, Xu L, Hicklin DJ, Fukumura D, di Tomaso E et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation. Cancer Cell 2004;6(6):553-563; PMID: 15607960; http://dx.doi.org/10.1016/j.ccr.2004.10.011
  • Rivero S, Díaz-Guerra MJ, Monsalve EM, Laborda J, García-Ramírez JJ. DLK2 is a transcriptional target of KLF4 in the early stages of adipogenesis. J Mol Biol 2012;417(1-2):36-50; PMID:22306741; http://dx.doi.org/10.1016/j.jmb.2012.01.035
  • Rivero S, Ruiz-García A, Díaz-Guerra MJ, Laborda J, García-Ramírez JJ. Characterization of a proximal Sp1 response element in the mouse Dlk2 gene promoter. BMC Mol Biol 2011;12:52; PMID:22185379; http://dx.doi.org/10.1186/1471-2199-12-52
  • Culver C, Melvin A, Mudie S, Rocha S. HIF-1alpha depletion results in SP1-mediated cell cycle disruption and alters the cellular response to chemotherapeutic drugs. Cell Cycle 2011;10(8):1249-60; PMID:21412054; http://dx.doi.org/10.4161/cc.10.8.15326
  • Jean JC, George E, Kaestner KH, Brown LA, Spira A, Joyce-Brady M. Transcription factor Klf4, induced in the lung by oxygen at birth, regulates perinatal fibroblast and myofibroblast differentiation. PLoS One 2013;8(1):e54806; PMID:23372771 ; http://dx.doi.org/10.1371/journal.pone.0054806
  • Hofmann JJ, Iruela-Arispe ML. Notch signaling in blood vessels: who is talking to whom about what? Circ Res 2007;100(11):1556-68; PMID: 17556669; http://dx.doi.org/10.1161/01.RES.0000266408.42939.e4
  • Hellstrom M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson AK, Karlsson L, Gaiano N et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007;445(7129):776-80; PMID:17259973; http://dx.doi.org/10.1038/nature05571
  • Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD, Thurston G. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 2006;444(7122):1032-7; PMID:17183313; http://dx.doi.org/10.1038/nature05355
  • Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 2006;444(7122):1083-7; PMID:17183323; http://dx.doi.org/10.1038/nature05313
  • Rebay I, Fleming RJ, Fehon RG, Cherbas L, Cherbas P, Artavanis-Tsakonas S. Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 1991;67(4):687-99; PMID:1657403; http://dx.doi.org/10.1016/0092-8674(91)90064-6
  • Cordle J, Redfieldz C, Stacey M, Van der Merwe PA, Willis AC, Champion BR, Hambleton S, Handford PA. Localization of the delta-like-1-binding site in human Notch-1 and its modulation by calcium affinity. J Biol Chem 2008;283(17):11785-93; PMID:18296446; http://dx.doi.org/10.1074/jbc.M708424200
  • Reis M, Czupalla CJ, Ziegler N, Devraj K, Zinke J, Seidel S, Heck R, Thom S, Macas J, Bockamp E et al. Endothelial Wnt/β-catenin signaling inhibits glioma angiogenesis and normalizes tumor blood vessels by inducing PDGF-B expression. J Exp Med 2012;209(9):1611-27; PMID:22908324; http://dx.doi.org/10.1084/jem.20111580
  • Griffioen AW. Anti-angiogenesis: making the tumor vulnerable to the immune system. Cancer Immunol Immunother 2008;57(10): 1553-8; PMID:18438662; http://dx.doi.org/10.1007/s00262-008-0524-3
  • Bose A, Lowe DB, Rao A, Storkus WJ. Combined vaccine+axitinib therapy yields superior antitumor efficacy in a murine melanoma model. Melanoma Res 2012;22(3):236-43; PMID:22504156; http://dx.doi.org/10.1097/CMR.0b013e3283538293
  • Bose A, Taylor JL, Alber S, Watkins SC, Garcia JA, Rini BI, Ko JS, Cohen PA, Finke JH, Storkus WJ. Sunitinib facilitates the activation and recruitment of therapeutic anti-tumor immunity in concert with specific vaccination. Int J Cancer 2011;129(9):2158-70; PMID:21170961; http://dx.doi.org/10.1002/ijc.25863
  • Lowe DB, Bose A, Taylor JL, Tawbi H, Lin Y, Kirkwood JM, Storkus WJ. Dasatinib promotes the expansion of a therapeutically superior T-cell repertoire in response to dendritic cell vaccination against melanoma. Oncoimmunology 2014;3(1):e27589; PMID:24734217; http://dx.doi.org/10.4161/onci.27589
  • Finke JH, Rini B, Ireland J, Rayman P, Richmond A, Golshayan A, Wood L, Elson P, Garcia J, Dreicer R et al. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clinical cancer research : an official journal of the American Association for Cancer Research 2008;14(20):6674-82; PMID:18927310; http://dx.doi.org/10.1158/1078-0432.CCR-07-5212
  • Mrass P, Takano H, Ng LG, Daxini S, Lasaro MO, Iparraguirre A, Cavanagh LL, von Andrian UH, Ertl HC, Haydon PG et al. Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J Exp Med 2006;203(12):2749-2761; PMID:17116735; http://dx.doi.org/10.1084/jem.20060710
  • Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med 2007;204(2):345-356; PMID:17261634; http://dx.doi.org/10.1084/jem.20061890
  • Facciponte JG, Ugel S, De Sanctis F, Li C, Wang L, Nair G, Sehgal S, Raj A, Matthaiou E, Coukos G et al. Tumor endothelial marker 1-specific DNA vaccination targets tumor vasculature. J Clin Invest 2014;124(4):1497-511; PMID:24642465; http://dx.doi.org/10.1172/JCI67382
  • Seavey MM, Maciag PC, Al-Rawi N, Sewell D, Paterson Y. An anti-vascular endothelial growth factor receptor 2/fetal liver kinase-1 Listeria monocytogenes anti-angiogenesis cancer vaccine for the treatment of primary and metastatic Her-2/neu+ breast tumors in a mouse model. J Immunol 2009;182(9):5537-46; PMID:19380802; http://dx.doi.org/10.4049/jimmunol.0803742
  • Blattman JN, Wherry EJ, Ha SJ, Van der Most RG, Ahmed R. Impact of epitope escape on PD-1 expression and CD8 T-cell exhaustion during chronic infection. J Virol 2009;83(9):4386-94; PMID: 19211743; http://dx.doi.org/10.1128/JVI.02524-08
  • Spranger S, Spaapen RM, Zha Y, Williams J, Meng Y, Ha TT, Gajewski TF. Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Sci Transl Med 2013;5(200):200ra116; PMID:23986400; http://dx.doi.org/10.1126/scitranslmed.3006504
  • Jayaraman P, Sada-Ovalle I, Beladi S, Anderson AC, Dardalhon V, Hotta C, Kuchroo VK, Behar SM. Tim3 binding to galectin-9 stimulates antimicrobial immunity. J Exp Med 2010;207(11):2343-54; PMID:20937702; http://dx.doi.org/10.1084/jem.20100687

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