Cancer Research; Oncology; virotherapy; oncolytic herpesvirus; glioblastoma; nanobody
Research center :
GIGA-I3 - Giga-Infection, Immunity and Inflammation - ULiège
Disciplines :
Human health sciences: Multidisciplinary, general & others
Author, co-author :
Sanchez Gil, Judit; ULiège - Université de Liège [BE] > GIGA I3 > Virology and Immunology
Dubois, Maxime ; Université de Liège - ULiège > GIGA > GIGA I3 - Virology and Immunology
Neirinckx, Virginie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
LOMBARD, Arnaud ; Centre Hospitalier Universitaire de Liège - CHU > > Service de neurochirurgie
Coppieters't Wallant, Natacha ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Nervous system disorders and therapy
D'arrigo, Paolo ; Université de Liège - ULiège > Département des sciences de la vie > Virologie - Immunologie
Isci, Damla ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Aldenhoff, Thérèse ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Nervous system disorders and therapy
Brouwers, Benoît ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Lassence, Cédric ; Université de Liège - ULiège > Département des sciences de la vie
ROGISTER, Bernard ; Centre Hospitalier Universitaire de Liège - CHU > > Service de neurologie
Lebrun, Marielle ; Université de Liège - ULiège > Département des sciences de la vie > Virologie - Immunologie
Sadzot, Catherine ; Université de Liège - ULiège > Département des sciences de la vie > Virologie - Immunologie
Feng, Y., Broder, C.C., Kennedy, P.E., Berger, E.A., HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272 (1996), 872–877, 10.1126/science.272.5263.872.
Alimohammadi, M., Rahimi, A., Faramarzi, F., Alizadeh-Navaei, R., Rafiei, A., Overexpression of chemokine receptor CXCR4 predicts lymph node metastatic risk in patients with melanoma: a systematic review and meta-analysis. Cytokine, 148, 2021, 155691, 10.1016/j.cyto.2021.155691.
Salmaggi, A., Gelati, M., Pollo, B., Marras, C., Silvani, A., Balestrini, M.R., Eoli, M., Fariselli, L., Broggi, G., Boiardi, A., CXCL12 expression is predictive of a shorter time to tumor progression in low-grade glioma: a single-institution study in 50 patients. J. Neurooncol. 74 (2005), 287–293, 10.1007/s11060-004-7327-y.
Katsumoto, K., Kume, S., The role of CXCL12-CXCR4 signaling pathway in pancreatic development. Theranostics 3 (2013), 11–17, 10.7150/thno.4806.
Gagliardi, F., Narayanan, A., Reni, M., Franzin, A., Mazza, E., Boari, N., Bailo, M., Zordan, P., Mortini, P., The role of CXCR4 in highly malignant human gliomas biology: current knowledge and future directions. Glia 62 (2014), 1015–1023, 10.1002/glia.22669.
Santagata, S., Ieranò, C., Trotta, A.M., Capiluongo, A., Auletta, F., Guardascione, G., Scala, S., CXCR4 and CXCR7 signaling pathways: a focus on the cross-talk between cancer cells and tumor microenvironment. Front. Oncol., 11, 2021, 591386, 10.3389/fonc.2021.591386.
Gatti, M., Pattarozzi, A., Bajetto, A., Würth, R., Daga, A., Fiaschi, P., Zona, G., Florio, T., Barbieri, F., Inhibition of CXCL12/CXCR4 autocrine/paracrine loop reduces viability of human glioblastoma stem-like cells affecting self-renewal activity. Toxicology 314 (2013), 209–220, 10.1016/j.tox.2013.10.003.
Mercurio, L., Ajmone-Cat, M.A., Cecchetti, S., Ricci, A., Bozzuto, G., Molinari, A., Manni, I., Pollo, B., Scala, S., Carpinelli, G., Minghetti, L., Targeting CXCR4 by a selective peptide antagonist modulates tumor microenvironment and microglia reactivity in a human glioblastoma model. J. Exp. Clin. Cancer Res., 35, 2016, 55, 10.1186/s13046-016-0326-y.
Gil, M., Seshadri, M., Komorowski, M.P., Abrams, S.I., Kozbor, D., Targeting CXCL12/CXCR4 signaling with oncolytic virotherapy disrupts tumor vasculature and inhibits breast cancer metastases. Proc. Natl. Acad. Sci. U S A 110 (2013), E1291–E1300, 10.1073/pnas.1220580110.
Scala, S., Molecular pathways: targeting the CXCR4-CXCL12 Axis-Untapped potential in the tumor microenvironment. Clin. Cancer Res. 21 (2015), 4278–4285, 10.1158/1078-0432.ccr-14-0914.
Kioi, M., Vogel, H., Schultz, G., Hoffman, R.M., Harsh, G.R., Brown, J.M., Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 120 (2010), 694–705, 10.1172/jci40283.
Lee, C.C., Lai, J.H., Hueng, D.Y., Ma, H.I., Chung, Y.C., Sun, Y.Y., Tsai, Y.J., Wu, W.B., Chen, C.L., Disrupting the CXCL12/CXCR4 axis disturbs the characteristics of glioblastoma stem-like cells of rat RG2 glioblastoma. Cancer Cell Int., 13, 2013, 85, 10.1186/1475-2867-13-85.
Ostrom, Q.T., Gittleman, H., Truitt, G., Boscia, A., Kruchko, C., Barnholtz-Sloan, J.S., CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2011-2015. Neuro. Oncol. 20 (2018), 1–86, 10.1093/neuonc/noy131.
Stupp, R., Taillibert, S., Kanner, A., Read, W., Steinberg, D.M., Lhermitte, B., Toms, S., Idbaih, A., Ahluwalia, M.S., Fink, K., et al. Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA, 318, 2017, 2306, 10.1001/jama.2017.18718.
Lara-Velazquez, M., Al-Kharboosh, R., Jeanneret, S., Vazquez-Ramos, C., Mahato, D., Tavanaiepour, D., Rahmathulla, G., Quinones-Hinojosa, A., Advances in brain tumor surgery for glioblastoma in adults. Brain Sci., 7, 2017, 166, 10.3390/brainsci7120166.
Galli, R., Binda, E., Orfanelli, U., Cipelletti, B., Gritti, A., De Vitis, S., Fiocco, R., Foroni, C., Dimeco, F., Vescovi, A., Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64 (2004), 7011–7021, 10.1158/0008-5472.can-04-1364.
Chen, R., Nishimura, M.C., Bumbaca, S.M., Kharbanda, S., Forrest, W.F., Kasman, I.M., Greve, J.M., Soriano, R.H., Gilmour, L.L., Rivers, C.S., et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 17 (2010), 362–375, 10.1016/j.ccr.2009.12.049.
Singh, S.K., Clarke, I.D., Terasaki, M., Bonn, V.E., Hawkins, C., Squire, J., Dirks, P.B., Identification of a cancer stem cell in human brain tumors. Cancer Res. 63 (2003), 5821–5828.
Goffart, N., Kroonen, J., Di Valentin, E., Dedobbeleer, M., Denne, A., Martinive, P., Rogister, B., Adult mouse subventricular zones stimulate glioblastoma stem cells specific invasion through CXCL12/CXCR4 signaling. Neuro. Oncol. 17 (2015), 81–94, 10.1093/neuonc/nou144.
Goffart, N., Lombard, A., Lallemand, F., Kroonen, J., Nassen, J., Di Valentin, E., Berendsen, S., Dedobbeleer, M., Willems, E., Robe, P., et al. CXCL12 mediates glioblastoma resistance to radiotherapy in the subventricular zone. Neuro. Oncol. 19 (2017), 66–77, 10.1093/neuonc/now136.
Dedobbeleer, M., Willems, E., Lambert, J., Lombard, A., Digregorio, M., Lumapat, P.N., Di Valentin, E., Freeman, S., Goffart, N., Scholtes, F., Rogister, B., MKP1 phosphatase is recruited by CXCL12 in glioblastoma cells and plays a role in DNA strand breaks repair. Carcinogenesis 41 (2020), 417–429, 10.1093/carcin/bgz151.
Cheray, M., Bégaud, G., Deluche, E., Nivet, A., Battu, S., Lalloué, F., et al. Cancer stem-like cells in glioblastoma. De Vleeschouwer, S., (eds.) Glioblastoma, Chapter 4, 2017, Codon Publications, 59–71.
Lombard, A., Digregorio, M., Delcamp, C., Rogister, B., Piette, C., Coppieters, N., The subventricular zone, a hideout for adult and pediatric high-grade glioma stem cells. Front. Oncol., 10, 2020, 614930, 10.3389/fonc.2020.614930.
Tang, X., Zuo, C., Fang, P., Liu, G., Qiu, Y., Huang, Y., Tang, R., Targeting glioblastoma stem cells: a review on biomarkers, signal pathways and targeted therapy. Front. Oncol., 11, 2021, 701291, 10.3389/fonc.2021.701291.
Fountzilas, C., Patel, S., Mahalingam, D., Review: oncolytic virotherapy, updates and future directions. Oncotarget 8 (2017), 102617–102639, 10.18632/oncotarget.18309.
Miyauchi, J.T., Tsirka, S.E., Advances in immunotherapeutic research for glioma therapy. J. Neurol. 265 (2018), 741–756, 10.1007/s00415-017-8695-5.
Friedman, G.K., Langford, C.P., Coleman, J.M., Cassady, K.A., Parker, J.N., Markert, J.M., Yancey Gillespie, G., Engineered herpes simplex viruses efficiently infect and kill CD133+ human glioma xenograft cells that express CD111. J. Neuro. Oncol. 95 (2009), 199–209, 10.1007/s11060-009-9926-0.
Rueger, M.A., Winkeler, A., Miletic, H., Kaestle, C., Richter, R., Schneider, G., Hilker, R., Heneka, M.T., Ernestus, R.I., Hampl, J.A., et al. Variability in infectivity of primary cell cultures of human brain tumors with HSV-1 amplicon vectors. Gene Ther. 12 (2005), 588–596, 10.1038/sj.gt.3302462.
Menotti, L., Nicoletti, G., Gatta, V., Croci, S., Landuzzi, L., De Giovanni, C., Nanni, P., Lollini, P.-L., Campadelli-Fiume, G., Inhibition of human tumor growth in mice by an oncolytic herpes simplex virus designed to target solely HER-2-positive cells. Proc. Natl. Acad. Sci. U S A 106 (2009), 9039–9044, 10.1073/pnas.0812268106.
Kamiyama, H., Zhou, G., Roizman, B., Herpes simplex virus 1 recombinant virions exhibiting the amino terminal fragment of urokinase-type plasminogen activator can enter cells via the cognate receptor. Gene Ther. 13 (2006), 621–629, 10.1038/sj.gt.3302685.
Zhou, G., Roizman, B., Construction and properties of a herpes simplex virus 1 designed to enter cells solely via the IL-13α2 receptor. Proc. Natl. Acad. Sci. U S A 103 (2006), 5508–5513, 10.1073/pnas.0601258103.
Grandi, P., Fernandez, J., Szentirmai, O., Carter, R., Gianni, D., Sena-Esteves, M., Breakefield, X.O., Targeting HSV-1 virions for specific binding to epidermal growth factor receptor-vIII-bearing tumor cells. Cancer Gene Ther. 17 (2010), 655–663, 10.1038/cgt.2010.22.
Shibata, T., Uchida, H., Shiroyama, T., Okubo, Y., Suzuki, T., Ikeda, H., Yamaguchi, M., Miyagawa, Y., Fukuhara, T., Cohen, J.B., et al. Development of an oncolytic HSV vector fully retargeted specifically to cellular EpCAM for virus entry and cell-to-cell spread. Gene Ther. 23 (2016), 479–488, 10.1038/gt.2016.17.
Alessandrini, F., Menotti, L., Avitabile, E., Appolloni, I., Ceresa, D., Marubbi, D., Campadelli-Fiume, G., Malatesta, P., Eradication of glioblastoma by immuno-virotherapy with a retargeted oncolytic HSV in a preclinical model. Oncogene 38 (2019), 4467–4479, 10.1038/s41388-019-0737-2.
Jahan, N., Lee, J.M., Shah, K., Wakimoto, H., Therapeutic targeting of chemoresistant and recurrent glioblastoma stem cells with a proapoptotic variant of oncolytic herpes simplex virus. Int. J. Cancer 141 (2017), 1671–1681, 10.1002/ijc.30811.
Kim, M.-H., Billiar, T.R., Seol, D.-W., The secretable form of trimeric TRAIL, a potent inducer of apoptosis. Biochem. Biophys. Res. Commun. 321 (2004), 930–935, 10.1016/j.bbrc.2004.07.046.
Kock, N., Kasmieh, R., Weissledery, R., Shah, K., Tumor therapy mediated by lentiviral expression of shBcl-2 and S-TRAIL. Neoplasia 9 (2007), 435–442, 10.1593/neo.07223.
Tamura, K., Wakimoto, H., Agarwal, A.S., Rabkin, S.D., Bhere, D., Martuza, R.L., Kuroda, T., Kasmieh, R., Shah, K., Multimechanistic tumor targeted oncolytic virus overcomes resistance in brain tumors. Mol. Ther. 21 (2013), 68–77, 10.1038/mt.2012.175.
Wakimoto, H., Kesari, S., Farrell, C.J., Curry, W.T., Zaupa, C., Aghi, M., Kuroda, T., Stemmer-Rachamimov, A., Shah, K., Liu, T.C., et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res. 69 (2009), 3472–3481, 10.1158/0008-5472.can-08-3886.
WO2016156570A1- Bispecific CXCR4-CD4 polypeptides with potent anti-HIV activity (https://patents.google.com/patent/WO2016156570A1/en?oq=WO2016156570) Google Patents 2016.
Uchida, H., Marzulli, M., Nakano, K., Goins, W.F., Chan, J., Hong, C.-S., Mazzacurati, L., Yoo, J.Y., Haseley, A., Nakashima, H., et al. Effective treatment of an orthotopic xenograft model of human glioblastoma using an EGFR-retargeted oncolytic herpes simplex virus. Mol. Ther. 21 (2013), 561–569, 10.1038/mt.2012.211.
Uchida, H., Chan, J., Goins, W.F., Grandi, P., Kumagai, I., Cohen, J.B., Glorioso, J.C., A double mutation in glycoprotein gB compensates for ineffective gD-dependent initiation of herpes simplex virus type 1 infection. J. Virol. 84 (2010), 12200–12209, 10.1128/jvi.01633-10.
Shah, K., Tung, C.H., Yang, K., Weissleder, R., Breakefield, X.O., Inducible release of TRAIL fusion proteins from a proapoptotic form for tumor therapy. Cancer Res. 64 (2004), 3236–3242, 10.1158/0008-5472.can-03-3516.
Cocchi, F., Menotti, L., Mirandola, P., Lopez, M., Campadelli-Fiume, G., The ectodomain of a novel member of the Immunoglobulin subfamily related to the poliovirus receptor has the attributes of a bona fide receptor for herpes simplex virus types 1 and 2 in human cells. J. Virol. 72 (1998), 9992–10002, 10.1128/jvi.72.12.9992-10002.1998.
Uchida, H., Shah, W.A., Ozuer, A., Frampton, A.R., Goins, W.F., Grandi, P., Cohen, J.B., Glorioso, J.C., Glorioso, J.C., Generation of herpesvirus entry mediator (HVEM)-Restricted herpes simplex virus type 1 mutant viruses: resistance of HVEM-expressing cells and identification of mutations that rescue nectin-1 recognition. J. Virol. 83 (2009), 2951–2961, 10.1128/jvi.01449-08.
Frampton, A.R., Stolz, D.B., Uchida, H., Goins, W.F., Cohen, J.B., Glorioso, J.C., Equine herpesvirus 1 enters cells by two different pathways, and infection requires the activation of the cellular kinase ROCK1. J. Virol. 81 (2007), 10879–10889, 10.1128/jvi.00504-07.
Marconi, P., Manservigi, R., Herpes simplex virus growth, preparation, and assay. Methods Mol. Biol. 1144 (2014), 19–29, 10.1007/978-1-4939-0428-0_2.
Connolly, S.A., Jardetzky, T.S., Longnecker, R., The structural basis of herpesvirus entry. Nat. Rev. Microbiol. 19 (2021), 110–121, 10.1038/s41579-020-00448-w.
Bian, X.w., Yang, S.x., Chen, J.h., Ping, Y.f., Zhou, X.d., Wang, Q.l., Jiang, X.f., Gong, W., Xiao, H.l., Du, L.l., et al. Preferantial expression of chemokine receptor CXCR4 by highly malignant human gliomas and its association with poor patient survival. Neurosurgery 61 (2007), 570–579, 10.1227/01.neu.0000290905.53685.a2.
Tang, C., Guo, W., Implantation of a mini-osmotic pump plus stereotactical injection of retrovirus to study newborn neuron development in adult mouse hippocampus. STAR Protoc., 2, 2021, 100374, 10.1016/j.xpro.2021.100374.
Alvarez-Breckenridge, C.A., Yu, J., Price, R., Wojton, J., Pradarelli, J., Mao, H., Wei, M., Wang, Y., He, S., Hardcastle, J., et al. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat. Med. 18 (2012), 1827–1834, 10.1038/nm.3013.
Van Den Bossche, W.B.L., Kleijn, A., Teunissen, C.E., Voerman, J.S.A., Teodosio, C., Noske, D.P., Van Dongen, J.J.M., Dirven, C.M.F., Lamfers, M.L.M., Oncolytic virotherapy in glioblastoma patients induces a tumor macrophage phenotypic shift leading to an altered glioblastoma microenvironment. Neuro. Oncol. 20 (2018), 1494–1504, 10.1093/neuonc/noy082.
Isci, D., D'uonnolo, G., Wantz, M., Rogister, B., Lombard, A., Chevigné, A., Szpakowska, M., Neirinckx, V., Patient-oriented perspective on chemokine receptor expression and function in glioma. Cancers, 14, 2021, 130, 10.3390/cancers14010130.
Tischer, B.K., Kaufer, B.B., Sommer, M., Wussow, F., Arvin, A.M., Osterrieder, N., A self-excisable infectious bacterial artificial chromosome clone of varicella-zoster virus allows analysis of the essential tegument protein encoded by ORF9. J. Virol. 81 (2007), 13200–13208, 10.1128/jvi.01148-07.
Todo, T., Martuza, R.L., Rabkin, S.D., Johnson, P.A., Oncolytic herpes simplex virus vector with enhanced MHC class I presentation and tumor cell killing. Proc. Natl. Acad. Sci. U S A 98 (2001), 6396–6401, 10.1073/pnas.101136398.
Kroonen, J., Nassen, J., Boulanger, Y.G., Provenzano, F., Capraro, V., Bours, V., Martin, D., Deprez, M., Robe, P., Rogister, B., Human glioblastoma-initiating cells invade specifically the subventricular zones and olfactory bulbs of mice after striatal injection. Int. J. Cancer 129 (2011), 574–585, 10.1002/ijc.25709.