Interleukin 4 and cancer resistance in glioblastoma multiforme.
Cancer
Glioblastoma
Hallmarks
Immunotherapy
Interleukin
Journal
Neurosurgical review
ISSN: 1437-2320
Titre abrégé: Neurosurg Rev
Pays: Germany
ID NLM: 7908181
Informations de publication
Date de publication:
21 Aug 2024
21 Aug 2024
Historique:
received:
30
07
2024
accepted:
11
08
2024
revised:
30
07
2024
medline:
21
8
2024
pubmed:
21
8
2024
entrez:
20
8
2024
Statut:
epublish
Résumé
In this review, the author highlights the role of IL4 in mitigating all the "hallmarks" of cancer growth and resistance to current immunotherapy, providing a framework for its role in GBM as well as guideline for future treatment regimens. This review is organized around six strategies by which IL4 contributes to the immune resistance seen in GBM: (i) apoptosis evasion, (ii) self-sufficiency in growth signals, (iii) insensitivity to anti-growth signals, (iv) invasion and metastasis, (v) limitless replicative potential, (vi) sustained angiogenesis.
Identifiants
pubmed: 39164434
doi: 10.1007/s10143-024-02695-4
pii: 10.1007/s10143-024-02695-4
doi:
Substances chimiques
Interleukin-4
207137-56-2
IL4 protein, human
0
Types de publication
Journal Article
Review
Letter
Langues
eng
Sous-ensembles de citation
IM
Pagination
448Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Dunn GP, Old LJ, Schreiber RD (2004) The three Es of cancer immunoediting. Annu Rev Immunol 22:329–360
pubmed: 15032581
Jackson CM, Choi J, Lim M (2019) Mechanisms of immunotherapy resistance: lessons from glioblastoma. Nat Immunol 20(9):1100–1109
pubmed: 31358997
Louis DN, Perry A, Reifenberger G et al (2016) The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol 131(6):803–820
pubmed: 27157931
Ostrom QT, Gittleman H, Farah P et al (2013) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2006–2010. Neurooncology 15(suppl2):ii1–ii56
Tamimi AF, Juweid M Epidemiology and outcome of glioblastoma. Exon Publications. 2017:143–153
Pearson JR, Regad T (2017) Targeting cellular pathways in glioblastoma multiforme. Signal Transduct Target Therapy 2(1):1–11
Weller M, Butowski N, Tran DD et al (2017) Rindopepimut with temozolomide for patients with newly diagnosed, EGFRvIII-expressing glioblastoma (ACT IV): a randomised, double-blind, international phase 3 trial. Lancet Oncol 18(10):1373–1385
pubmed: 28844499
Omuro A, Vlahovic G, Lim M et al (2018) Nivolumab with or without ipilimumab in patients with recurrent glioblastoma: results from exploratory phase I cohorts of CheckMate 143. Neurooncology 20(5):674–686
Stupp R, Mason WP, Van Den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996
pubmed: 15758009
Koshy M, Villano JL, Dolecek TA et al (2012) Improved survival time trends for glioblastoma using the SEER 17 population-based registries. J Neurooncol 107(1):207–212
pubmed: 21984115
Nelms K, Keegan AD, Zamorano J, Ryan JJ, Paul WE (1999) The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 17(1):701–738
pubmed: 10358772
Jiang H, Harris MB, Rothman P (2000) Il-4/il-13 signaling beyond jak/stat. J Allergy Clin Immunol 105(6):1063–1070
pubmed: 10856136
Scheurer ME, Amirian E, Cao Y et al (2008) Polymorphisms in the interleukin-4 receptor gene are associated with better survival in patients with glioblastoma. Clin Cancer Res 14(20):6640–6646
pubmed: 18927306
pmcid: 2995250
Eisele G, Weller M (2013) Targeting apoptosis pathways in glioblastoma. Cancer Lett 332(2):335–345
pubmed: 21269762
Kruse J-P, Gu W (2009) Modes of p53 regulation. Cell 137(4):609–622
pubmed: 19450511
pmcid: 3737742
Farnebo M, Bykov VJ, Wiman KG (2010) The p53 tumor suppressor: a master regulator of diverse cellular processes and therapeutic target in cancer. Biochem Biophys Res Commun 396(1):85–89
pubmed: 20494116
Leonard WJ, O’Shea JJ (1998) Jaks and STATs: biological implications. Annu Rev Immunol 16(1):293–322
pubmed: 9597132
Miyazaki T, Kawahara A, Fujii H et al (1994) Functional activation of Jak1 and Jak3 by selective association with IL-2 receptor subunits. Science 266(5187):1045–1047
pubmed: 7973659
Rahaman SO, Sharma P, Harbor PC, Aman MJ, Vogelbaum MA, Haque SJ (2002) IL-13Rα2, a decoy receptor for IL-13 acts as an inhibitor of IL-4-dependent signal transduction in glioblastoma cells. Cancer Res 62(4):1103–1109
pubmed: 11861389
Rahaman SO, Harbor PC, Chernova O, Barnett GH, Vogelbaum MA, Haque SJ (2002) Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene 21(55):8404–8413
pubmed: 12466961
Niu G, Wright KL, Huang M et al (2002) Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 21(13):2000–2008
pubmed: 11960372
Cheng F, Wang H-W, Cuenca A et al (2003) A critical role for Stat3 signaling in immune tolerance. Immunity 19(3):425–436
pubmed: 14499117
Wang T, Niu G, Kortylewski M et al (2004) Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat Med 10(1):48–54
pubmed: 14702634
Yu H, Jove R (2004) The STATs of cancer—new molecular targets come of age. Nat Rev Cancer 4(2):97–105
pubmed: 14964307
Arima K, Sato K, Tanaka G et al (2005) Characterization of the interaction between interleukin-13 and interleukin-13 receptors. J Biol Chem 280(26):24915–24922
pubmed: 15870068
Nijhawan D, Fang M, Traer E et al (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev 17(12):1475–1486
pubmed: 12783855
pmcid: 196078
Thallinger C, Wolschek MF, Wacheck V et al (2003) Mcl-1 antisense therapy chemosensitizes human melanoma in a SCID mouse xenotransplantation model. J Invest Dermatology 120(6):1081–1086
Edin S, Wikberg ML, Rutegård J, Oldenborg P-A, Palmqvist R (2013) Phenotypic skewing of macrophages in vitro by secreted factors from colorectal cancer cells. PLoS ONE 8(9):e74982
pubmed: 24058644
pmcid: 3776729
Koenig A, Vilsmaier T, Rack B et al (2016) Determination of interleukin-4,-5,-6,-8 and-13 in serum of patients with breast cancer before treatment and its correlation to circulating tumor cells. Anticancer Res 36(6):3123–3130
Bouhlel MA, Derudas B, Rigamonti E et al (2007) PPARγ activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metabol 6(2):137–143
Guo B, Li L, Guo J et al (2017) M2 tumor-associated macrophages produce interleukin-17 to suppress oxaliplatin-induced apoptosis in hepatocellular carcinoma. Oncotarget 8(27):44465
pubmed: 28591705
pmcid: 5546494
Green DR, Kroemer G (2009) Cytoplasmic functions of the tumour suppressor p53. Nature 458(7242):1127–1130
pubmed: 19407794
pmcid: 2814168
Li L, Ng D, Mah W et al (2015) A unique role for p53 in the regulation of M2 macrophage polarization. Cell Death Differ 22(7):1081–1093
pubmed: 25526089
PESCH J, BREHM U, GRUMMT STAIBC (1996) Repression of interleukin-2 and interleukin-4 promoters by tumor suppressor protein p53. J Interferon Cytokine Res 16(8):595–600
pubmed: 8877730
Network CGAR (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455(7216):1061
Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57–70
pubmed: 10647931
Fedi P, Tronick S, Aaronson S (1997) Growth factors. Cancer Med. :41–64
Ruoslahti FGG (1999) Integrin signaling. Science 285(5430):1028–1032
pubmed: 10446041
Medema RH, Bos JL (1993) The role of p21ras in receptor tyrosine kinase signaling. Crit Rev Oncog 4(6):615–661
pubmed: 8286433
Hall WA, Fodstad Ø (1992) Immunotoxins and central nervous system neoplasia. J Neurosurg 76(1):1–12
pubmed: 1727147
Laske DW, Ilercil O, Akbasak A, Youle RJ, Oldfield EH (1994) Efficacy of direct intratumoral therapy with targeted protein toxins for solid human gliomas in nude mice. J Neurosurg 80(3):520–526
pubmed: 8113865
Husain SR, Behari N, Kreitman RJ, Pastan I, Puri RK (1998) Complete regression of established human glioblastoma tumor xenograft by interleukin-4 toxin therapy. Cancer Res 58(16):3649–3653
pubmed: 9721874
Huang PH, Xu AM, White FM (2009) Oncogenic EGFR signaling networks in glioma. Sci Signal 2(87):re6–re6
pubmed: 19738203
Zhang C, Burger MC, Jennewein L et al (2016) ErbB2/HER2-specific NK cells for targeted therapy of glioblastoma. J Natl Cancer Inst 108(5):djv375
Jahani-Asl A, Yin H, Soleimani VD et al (2016) Control of glioblastoma tumorigenesis by feed-forward cytokine signaling. Nat Neurosci 19(6):798–806
pubmed: 27110918
pmcid: 4984527
Guo Q, Guan Gf C, Jy et al (2019) Overexpression of oncostatin M receptor regulates local immune response in glioblastoma. J Cell Physiol 234(9):15496–15509
pubmed: 30693511
Newman JP, Wang GY, Arima K et al (2017) Interleukin-13 receptor alpha 2 cooperates with EGFRvIII signaling to promote glioblastoma multiforme. Nat Commun 8(1):1–17
Itoh N, Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20(11):563–569
pubmed: 15475116
Bohrer LR, Chuntova P, Bade LK et al (2014) Activation of the FGFR–STAT3 pathway in breast cancer cells induces a hyaluronan-rich microenvironment that licenses tumor formation. Cancer Res 74(1):374–386
pubmed: 24197137
Wang A, de la Motte C, Lauer M, Hascall V (2011) Hyaluronan matrices in pathobiological processes. FEBS J 278(9):1412–1418
pubmed: 21362136
pmcid: 4401461
Cecchi F, Rabe C, Bottaro DP (2011) The hepatocyte growth factor receptor: structure, function and pharmacological targeting in cancer. Curr Signal Transduct Ther 6(2):146–151
pubmed: 25197268
pmcid: 4156285
Brennan CW, Verhaak RG, McKenna A et al (2013) The somatic genomic landscape of glioblastoma. Cell 155(2):462–477
pubmed: 24120142
pmcid: 3910500
Kong DS, Song SY, Kim DH et al (2009) Prognostic significance of c-Met expression in glioblastomas. Cancer 115(1):140–148
pubmed: 18973197
Petterson SA, Dahlrot RH, Hermansen SK et al (2015) High levels of c-Met is associated with poor prognosis in glioblastoma. J Neurooncol 122(3):517–527
pubmed: 25800004
Day RM, Soon L, Breckenridge D et al (2002) Mitogenic synergy through multilevel convergence of hepatocyte growth factor and interleukin-4 signaling pathways. Oncogene 21(14):2201–2211
pubmed: 11948403
Baskin DG, Wilcox BJ, Figlewicz DP, Dorsa DM (1988) Insulin and insulin-like growth factors in the CNS. Trends Neurosci 11(3):107–111
pubmed: 2465607
Sara VR, Carlsson-Skwirut C (1988) The role of the insulin-like growth factors in the regulation of brain development. Prog Brain Res 73:87–99
pubmed: 3047812
Glick RP, Lichtor T, Unterman TG (1997) Insulin-like growth factors in central nervous system tumors. J Neurooncol 35(3):315–325
pubmed: 9440028
Prisell P, Persson L, Boethius J, Sara V (1987) Somatomedins in tumour cyst fluid, cerebrospinal fluid, and tumour cytosol in patients with glial tumours. Acta Neurochir 89(1):48–52
pubmed: 3434342
Sandberg A-C, Engberg C, Lake M, von Holst H, Sara VR (1988) The expression of insulin-like growth factor I and insulin-like growth factor II genes in the human fetal and adult brain and in glioma. Neurosci Lett 93(1):114–119
pubmed: 3211366
Lichtor T, Kurpakus MA, Gurney ME (1991) Differential expression of insulin-like growth factor II in human meningiomas. Neurosurgery 29(3):405–410
pubmed: 1656313
Antoniades HN, Galanopoulos T, Neville-Golden J, Maxwell M (1992) Expression of insulin‐like growth factors I and II and their receptor mRNAs in primary human astrocytomas and meningiomas; in vivo studies using in situ hybridization and immunocytochemistry. Int J Cancer 50(2):215–222
pubmed: 1370435
Saka VR, Hall K, Von Holtz H, Humbel R, Sjören B, Wetterberg L (1982) Evidence for the presence of specific receptors for insulin-like growth factors 1 (IGF-1) and 2 (IGF-2) and insulin throughout the adult human brain. Neurosci Lett 34(1):39–44
Gammeltoft S, Haselbacher G, Humbel R, Fehlmann M, Van Obberghen E (1985) Two types of receptor for insulin-like growth factors in mammalian brain. EMBO J 4(13A):3407–3412
pubmed: 3004958
pmcid: 554677
Sandberg-Nordqvist A-C, Ståhlbom P-A, Reinecke M, Collins VP, von Holst H, Sara V (1993) Characterization of insulin-like growth factor 1 in human primary brain tumors. Cancer Res 53(11):2475–2478
pubmed: 8495408
Schlenska-Lange A, Knüpfer H, Lange TJ, Kiess W, Knüpfer M (2008) Cell proliferation and migration in glioblastoma multiforme cell lines are influenced by insulin-like growth factor I in vitro. Anticancer Res 28(2A):1055–1060
pubmed: 18507054
Maris C, D’Haene N, Trépant A-L et al (2015) IGF-IR: a new prognostic biomarker for human glioblastoma. Br J Cancer 113(5):729–737
pubmed: 26291053
pmcid: 4559821
Quail DF, Bowman RL, Akkari L et al (2016) The tumor microenvironment underlies acquired resistance to CSF-1R inhibition in gliomas. Science. ;352(6288)
Hermanson M, Funa K, Hartman M et al (1992) Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 52(11):3213–3219
pubmed: 1317261
Lokker NA, Sullivan CM, Hollenbach SJ, Israel MA, Giese NA (2002) Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res 62(13):3729–3735
pubmed: 12097282
Nazarenko I, Hede S-M, He X et al (2012) PDGF and PDGF receptors in glioma. Ups J Med Sci 117(2):99–112
pubmed: 22509804
pmcid: 3339542
Carmeliet P, Ferreira V, Breier G et al (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380(6573):435–439
pubmed: 8602241
Huang H, Lavoie-Lamoureux A, Moran K, Lavoie J-P (2007) IL-4 stimulates the expression of CXCL-8, E-selectin, VEGF, and inducible nitric oxide synthase mRNA by equine pulmonary artery endothelial cells. Am J Physiology-Lung Cell Mol Physiol 292(5):L1147–L1154
Lamagna C, Aurrand-Lions M, Imhof BA (2006) Dual role of macrophages in tumor growth and angiogenesis. J Leukoc Biol 80(4):705–713
pubmed: 16864600
Zhang B, Zhang Y, Yao G et al (2012) M2-polarized macrophages promote metastatic behavior of Lewis lung carcinoma cells by inducing vascular endothelial growth factor-C expression. Clinics 67:901–906
pubmed: 22948457
pmcid: 3416895
Moses HL, Yang EY, Pietenpol JA (1990) TGF-β stimulation and inhibition of cell proliferation: new mechanistic insights. Cell 63(2):245–247
pubmed: 2208284
Hannon GJ, Beach D (1994) pl5 INK4B is a potentia| effector of TGF-β-induced cell cycle arrest. Nature 371(6494):257–261
pubmed: 8078588
Datto MB, Hu PP-c, Kowalik TF, Yingling J, Wang X-F (1997) The viral oncoprotein E1A blocks transforming growth factor beta-mediated induction of p21/WAF1/Cip1 and p15/INK4B. Mol Cell Biol 17(4):2030–2037
pubmed: 9121451
pmcid: 232050
Weinberg RA (1995) The retinoblastoma protein and cell cycle control. Cell 81(3):323–330
pubmed: 7736585
Amin AR, Karpowicz PA, Carey TE et al (2015) Evasion of anti-growth signaling: a key step in tumorigenesis and potential target for treatment and prophylaxis by natural compounds. Elsevier, pp S55–S77
Macey MR, Sturgill JL, Morales JK et al (2010) IL-4 and TGF-β1 counterbalance one another while regulating mast cell homeostasis. J Immunol 184(9):4688–4695
pubmed: 20304823
Mimeault M, Batra SK (2010) Divergent molecular mechanisms underlying the pleiotropic functions of macrophage inhibitory cytokine-1 in cancer. J Cell Physiol 224(3):626–635
pubmed: 20578239
pmcid: 2932466
Wang X, Baek SJ, Eling TE (2013) The diverse roles of nonsteroidal anti-inflammatory drug activated gene (NAG-1/GDF15) in cancer. Biochem Pharmacol 85(5):597–606
pubmed: 23220538
Costa VL, Henrique R, Danielsen SA et al (2010) Three epigenetic biomarkers, GDF15, TMEFF2, and VIM, accurately predict bladder cancer from DNA-based analyses of urine samples. Clin Cancer Res 16(23):5842–5851
pubmed: 20975101
Welsh JB, Sapinoso LM, Kern SG et al (2003) Large-scale delineation of secreted protein biomarkers overexpressed in cancer tissue and serum. Proceedings of the National Academy of Sciences. ;100(6):3410–3415
Brown DA, Ward RL, Buckhaults P et al (2003) MIC-1 serum level and genotype: associations with progress and prognosis of colorectal carcinoma. Clin Cancer Res 9(7):2642–2650
pubmed: 12855642
Bock AJ, Stavnes HT, Kempf T et al (2010) Expression and clinical role of growth differentiation factor-15 in ovarian carcinoma effusions. Int J Gynecologic Cancer. ;20(9)
Staff AC, Bock AJ, Becker C, Kempf T, Wollert KC, Davidson B (2010) Growth differentiation factor-15 as a prognostic biomarker in ovarian cancer. Gynecol Oncol 118(3):237–243
pubmed: 20576287
Griner SE, Joshi JP, Nahta R (2013) Growth differentiation factor 15 stimulates rapamycin-sensitive ovarian cancer cell growth and invasion. Biochem Pharmacol 85(1):46–58
pubmed: 23085437
Koopmann J, Buckhaults P, Brown DA et al (2004) Serum macrophage inhibitory cytokine 1 as a marker of pancreatic and other periampullary cancers. Clin Cancer Res 10(7):2386–2392
pubmed: 15073115
Koopmann J, Rosenzweig CNW, Zhang Z et al (2006) Serum markers in patients with resectable pancreatic adenocarcinoma: macrophage inhibitory cytokine 1 versus CA19-9. Clin Cancer Res 12(2):442–446
pubmed: 16428484
Bauskin AR, Brown DA, Junankar S et al (2005) The propeptide mediates formation of stromal stores of PROMIC-1: role in determining prostate cancer outcome. Cancer Res 65(6):2330–2336
pubmed: 15781647
Brown DA, Stephan C, Ward RL et al (2006) Measurement of serum levels of macrophage inhibitory cytokine 1 combined with prostate-specific antigen improves prostate cancer diagnosis. Clin Cancer Res 12(1):89–96
pubmed: 16397029
Selander KS, Brown DA, Sequeiros GB et al (2007) Serum macrophage inhibitory cytokine-1 concentrations correlate with the presence of prostate cancer bone metastases. Cancer Epidemiol Prev Biomarkers 16(3):532–537
Martinez JM, Sali T, Okazaki R et al (2006) Drug-induced expression of nonsteroidal anti-inflammatory drug-activated gene/macrophage inhibitory cytokine-1/prostate-derived factor, a putative tumor suppressor, inhibits tumor growth. J Pharmacol Exp Ther 318(2):899–906
pubmed: 16714403
Baek SJ, Okazaki R, Lee S-H et al (2006) Nonsteroidal anti-inflammatory drug-activated gene-1 over expression in transgenic mice suppresses intestinal neoplasia. Gastroenterology 131(5):1553–1560
pubmed: 17101328
Cekanova M, Lee S-H, Donnell RL et al (2009) Nonsteroidal anti-inflammatory drug-activated gene-1 expression inhibits urethane-induced pulmonary tumorigenesis in transgenic mice. Cancer Prev Res 2(5):450–458
Lambert JR, Kelly JA, Shim M et al (2006) Prostate derived factor in human prostate cancer cells: gene induction by vitamin D via a p53-dependent mechanism and inhibition of prostate cancer cell growth. J Cell Physiol 208(3):566–574
pubmed: 16741990
Jung S-B, Choi MJ, Ryu D et al (2018) Reduced oxidative capacity in macrophages results in systemic insulin resistance. Nat Commun 9(1):1–15
Shnaper S, Desbaillets I, Brown DA et al (2009) Elevated levels of MIC-1/GDF15 in the cerebrospinal fluid of patients are associated with glioblastoma and worse outcome. Int J Cancer 125(11):2624–2630
pubmed: 19521960
Roth P, Junker M, Tritschler I et al (2010) GDF-15 contributes to proliferation and immune escape of malignant gliomas. Clin Cancer Res 16(15):3851–3859
pubmed: 20534737
Codó P, Weller M, Kaulich K et al (2016) Control of glioma cell migration and invasiveness by GDF-15. Oncotarget 7(7):7732
pubmed: 26741507
pmcid: 4884950
Albertoni M, Shaw PH, Nozaki M et al (2002) Anoxia induces macrophage inhibitory cytokine-1 (MIC-1) in glioblastoma cells independently of p53 and HIF-1. Oncogene 21(27):4212–4219
pubmed: 12082608
Yoshioka H, Kamitani H, Watanabe T, Eling TE (2008) Nonsteroidal anti-inflammatory drug-activated gene (NAG-1/GDF15) expression is increased by the histone deacetylase inhibitor trichostatin A. J Biol Chem 283(48):33129–33137
pubmed: 18801729
pmcid: 2586275
Kadowaki M, Yoshioka H, Kamitani H, Watanabe T, Wade PA, Eling TE (2012) DNA methylation-mediated silencing of nonsteroidal anti‐inflammatory drug‐activated gene (NAG‐1/GDF15) in glioma cell lines. Int J Cancer 130(2):267–277
pubmed: 21437897
Strelau J, Schmeer C, Peterziel H et al (2008) Expression and putative functions of GDF-15, a member of the TGF-β superfamily, in human glioma and glioblastoma cell lines. Cancer Lett 270(1):30–39
pubmed: 18550273
Lee SE, Kang SG, Choi MJ et al (2017) Growth differentiation factor 15 mediates systemic glucose regulatory action of T-helper type 2 cytokines. Diabetes 66(11):2774–2788
pubmed: 28874416
Sporn MB (1996) The war on cancer. Lancet (London England) 347(9012):1377–1381
pubmed: 8637346
Kalluri R (2009) EMT: when epithelial cells decide to become mesenchymal-like cells. J Clin Investig 119(6):1417–1419
pubmed: 19487817
pmcid: 2689122
Marcucci F, Stassi G, De Maria R (2016) Epithelial–mesenchymal transition: a new target in anticancer drug discovery. Nat Rev Drug Discovery 15(5):311–325
pubmed: 26822829
Pulaski BA, Ostrand-Rosenberg S (1998) Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7. 1 cell-based tumor vaccines. Cancer Res 58(7):1486–1493
pubmed: 9537252
Lelekakis M, Moseley JM, Martin TJ et al (1999) A novel orthotopic model of breast cancer metastasis to bone. Clin Exp Metastasis 17(2):163–170
pubmed: 10411109
Vadevoo SMP, Kim J-E, Gunassekaran GR et al (2017) IL4 receptor–targeted proapoptotic peptide blocks Tumor Growth and Metastasis by enhancing Antitumor Immunity. Mol Cancer Ther 16(12):2803–2816
pubmed: 28878029
Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4(1):71–78
pubmed: 14708027
Lewis CE, Pollard JW (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res 66(2):605–612
pubmed: 16423985
Noy R, Pollard JW (2014) Tumor-associated macrophages: from mechanisms to therapy. Immunity 41(1):49–61
pubmed: 25035953
pmcid: 4137410
Ding J, Jin W, Chen C, Shao Z, Wu J (2012) Tumor associated macrophage× cancer cell hybrids may acquire cancer stem cell properties in breast cancer. PLoS ONE 7(7):e41942
pubmed: 22848668
pmcid: 3405038
Fan Q-M, Jing Y-Y, Yu G-F et al (2014) Tumor-associated macrophages promote cancer stem cell-like properties via transforming growth factor-beta1-induced epithelial–mesenchymal transition in hepatocellular carcinoma. Cancer Lett 352(2):160–168
pubmed: 24892648
Liu C-Y, Xu J-Y, Shi X-Y et al (2013) M2-polarized tumor-associated macrophages promoted epithelial–mesenchymal transition in pancreatic cancer cells, partially through TLR4/IL-10 signaling pathway. Lab Invest 93(7):844–854
pubmed: 23752129
Gocheva V, Wang H-W, Gadea BB et al (2010) IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev 24(3):241–255
pubmed: 20080943
pmcid: 2811826
Shay JW, Bacchetti S (1997) A survey of telomerase activity in human cancer. Eur J Cancer 33(5):787–791
pubmed: 9282118
Bryan TM, Cech TR (1999) Telomerase and the maintenance of chromosome ends. Curr Opin Cell Biol 11(3):318–324
pubmed: 10395557
Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR (1995) Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J 14(17):4240–4248
pubmed: 7556065
pmcid: 394507
Hakin-Smith V, Jellinek D, Levy D et al (2003) Alternative lengthening of telomeres and survival in patients with glioblastoma multiforme. Lancet 361(9360):836–838
pubmed: 12642053
Chen Y-J, Hakin-Smith V, Teo M et al (2006) Association of mutant TP53 with alternative lengthening of telomeres and favorable prognosis in glioma. Cancer Res 66(13):6473–6476
pubmed: 16818615
Royds JA, Al Nadaf S, Wiles AK et al (2011) The CDKN2A G500 allele is more frequent in GBM patients with no defined telomere maintenance mechanism tumors and is associated with poorer survival. PLoS ONE 6(10):e26737
pubmed: 22046342
pmcid: 3202568
Heaphy CM, Subhawong AP, Hong S-M et al (2011) Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes. Am J Pathol 179(4):1608–1615
pubmed: 21888887
pmcid: 3181356
Lötsch D, Ghanim B, Laaber M et al (2013) Prognostic significance of telomerase-associated parameters in glioblastoma: effect of patient age. Neurooncology 15(4):423–432
Igarashi H, Sakaguchi N (1997) Telomerase activity is induced in human peripheral B lymphocytes by the stimulation to antigen receptor. Blood J Am Soc Hematol 89(4):1299–1307
Ozawa T, Gryaznov SM, Hu LJ et al (2004) Antitumor effects of specific telomerase inhibitor GRN163 in human glioblastoma xenografts. Neurooncology 6(3):218–226
Marian CO, Cho SK, Mcellin BM et al (2010) The telomerase antagonist, imetelstat, efficiently targets glioblastoma tumor-initiating cells leading to decreased proliferation and tumor growth. Clin Cancer Res 16(1):154–163
pubmed: 20048334
pmcid: 2883447
Ferrandon S, Malleval C, El Hamdani B et al (2015) Telomerase inhibition improves tumor response to radiotherapy in a murine orthotopic model of human glioblastoma. Mol Cancer 14(1):1–5
Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86(3):353–364
pubmed: 8756718
Bouck N, Stellmach V, Hsu SC (1996) How tumors become angiogenic. Adv Cancer Res 69:135–174
pubmed: 8791681
Toi M, Harris AL, Bicknell R (1991) Interleukin-4 is a potent mitogen for capillary endothelium. Biochem Biophys Res Commun 174(3):1287–1293
pubmed: 1996992
Fukushi J-i, Morisaki T, Shono T et al (1998) Novel Biological functions of Interleukin-4: formation of tube-like structures by vascular endothelial Cellsin Vitroand Angiogenesisin Vivo. Biochem Biophys Res Commun 250(2):444–448
pubmed: 9753649
Bochner BS, Klunk DA, Sterbinsky SA, Coffman RL, Schleimer RP (1995) IL-13 selectively induces vascular cell adhesion molecule-1 expression in human endothelial cells. J Immunol 154(2):799–803
pubmed: 7529288
De Palma M (2012) Partners in crime: VEGF and IL-4 conscript tumour‐promoting macrophages. J Pathol 227(1):4–7
pubmed: 22367978
Knizetova P, Ehrmann J, Hlobilkova A et al (2008) Autocrine regulation of glioblastoma cell-cycle progression, viability and radioresistance through the VEGF-VEGFR2 (KDR) interplay. Cell Cycle 7(16):2553–2561
pubmed: 18719373
Sjöström S, Wibom C, Andersson U et al (2011) Genetic variations in VEGF and VEGFR2 and glioblastoma outcome. J Neurooncol 104(2):523–527
pubmed: 21191630
Hu-Li J, Shevach E, Mizuguchi J, Ohara J, Mosmann T, Paul W (1987) B cell stimulatory factor 1 (interleukin 4) is a potent costimulant for normal resting T lymphocytes. J Exp Med 165(1):157–172
pubmed: 3098893
Minshall C, Arkins S, Straza J et al (1997) IL-4 and insulin-like growth factor-I inhibit the decline in Bcl-2 and promote the survival of IL-3-deprived myeloid progenitors. J Immunol 159(3):1225–1232
pubmed: 9233617
Hsieh C-S, Heimberger AB, Gold JS, O’Garra A, Murphy KM (1992) Differential regulation of T helper phenotype development by interleukins 4 and 10 in an alpha beta T-cell-receptor transgenic system. Proc Natl Acad Sci 89(13):6065–6069
pubmed: 1385868
pmcid: 49438
Seder RA, Paul WE, Davis MM, Fazekas de St Groth B (1992) The presence of interleukin 4 during in vitro priming determines the lymphokine-producing potential of CD4 + T cells from T cell receptor transgenic mice. J Exp Med 176(4):1091–1098
pubmed: 1328464
Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3(1):23–35
pubmed: 12511873
Geha RS, Jabara HH, Brodeur SR (2003) The regulation of immunoglobulin E class-switch recombination. Nat Rev Immunol 3(9):721–732
pubmed: 12949496
Callard RE, Matthews DJ, Hibbert L (1996) IL-4 and IL-13 receptors: are they one and the same? Immunol Today 17(3):108–110
pubmed: 8820266
Gadani SP, Cronk JC, Norris GT, Kipnis J (2012) IL-4 in the brain: a cytokine to remember. J Immunol 189(9):4213–4219
pubmed: 23087426
Olver S, Apte S, Baz A, Kienzle N (2007) The duplicitous effects of interleukin 4 on tumour immunity: how can the same cytokine improve or impair control of tumour growth? Tissue Antigens 69(4):293–298
pubmed: 17389011
Debinski W, Gibo DM (2000) Molecular expression analysis of restrictive receptor for interleukin 13, a brain tumor-associated cancer/testis antigen. Mol Med 6(5):440–449
pubmed: 10952023
pmcid: 1949955
Mantovani A, Sica A (2010) Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 22(2):231–237
pubmed: 20144856