Review Topical Sections

Contributions of immune cell populations in the maintenance, progression, and therapeutic modalities of glioma

  • Received: 07 February 2018 Accepted: 19 March 2018 Published: 21 March 2018
  • Immunotherapies are becoming a promising strategy for malignant disease. Selectively directing host immune responses to target cancerous tissue is a milestone of human health care. The roles of the innate and adaptive immune systems in both cancer progression and elimination are now being realized. Defining the immune cell environment and identifying the contributions of each sub-population of these cells has lead to an understanding of the immunotherapeutic processes, and demonstrated the potential of the immune system to drive cancer shrinkage and sustained immunity against disease. Poorly treated diseases, such as high-grade glioma, suffer from lack of therapeutic efficacy and rapid progression. Immunotherapeutic success in other solid malignancies, such as melanoma, now provides the principals for which this treatment paradigm can be adapted for primary brain cancers. The central nervous system is complex, and relative contributions of immune sub-populations to high grade glioma progression are not fully characterized. Here, we summarize recent research in both animal and humans which add to the knowledge base of how innate and adaptive immune cells contribute to glioma progression, and outline work which has demonstrated their potential to elicit anti-tumorigenic responses. Additionally, we highlight Neuropilin 1, a cell surface receptor protein, describe its signaling functions in the context of immunity, and point to its potential to slow glioma progression.

    Citation: Michael D. Caponegro, Jeremy Tetsuo Miyauchi, Stella E. Tsirka. Contributions of immune cell populations in the maintenance, progression, and therapeutic modalities of glioma[J]. AIMS Allergy and Immunology, 2018, 2(1): 24-44. doi: 10.3934/Allergy.2018.1.24

    Related Papers:

  • Immunotherapies are becoming a promising strategy for malignant disease. Selectively directing host immune responses to target cancerous tissue is a milestone of human health care. The roles of the innate and adaptive immune systems in both cancer progression and elimination are now being realized. Defining the immune cell environment and identifying the contributions of each sub-population of these cells has lead to an understanding of the immunotherapeutic processes, and demonstrated the potential of the immune system to drive cancer shrinkage and sustained immunity against disease. Poorly treated diseases, such as high-grade glioma, suffer from lack of therapeutic efficacy and rapid progression. Immunotherapeutic success in other solid malignancies, such as melanoma, now provides the principals for which this treatment paradigm can be adapted for primary brain cancers. The central nervous system is complex, and relative contributions of immune sub-populations to high grade glioma progression are not fully characterized. Here, we summarize recent research in both animal and humans which add to the knowledge base of how innate and adaptive immune cells contribute to glioma progression, and outline work which has demonstrated their potential to elicit anti-tumorigenic responses. Additionally, we highlight Neuropilin 1, a cell surface receptor protein, describe its signaling functions in the context of immunity, and point to its potential to slow glioma progression.


    加载中
    [1] Wen PY, Kesari S (2008) Malignant gliomas in adults. New Engl J Med 359: 492–507. doi: 10.1056/NEJMra0708126
    [2] Brennan C, Momota H, Hambardzumyan D, et al. (2009) Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS One 4: e7752. doi: 10.1371/journal.pone.0007752
    [3] Verhaak RG, Hoadley KA, Purdom E, et al. (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98–110. doi: 10.1016/j.ccr.2009.12.020
    [4] 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: 803–820. doi: 10.1007/s00401-016-1545-1
    [5] Stupp R, Mason WP, Van dBMJ, et al. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl J Med 352: 987–996.
    [6] Quail DF, Joyce JA (2017) The microenvironmental landscape of brain tumors. Cancer Cell 31: 326–341. doi: 10.1016/j.ccell.2017.02.009
    [7] Lohr J, Ratliff T, Huppertz A, et al. (2011) Effector T-cell infiltration positively impacts survival of glioblastoma patients and is impaired by tumor-derived TGF-beta. Clin Cancer Res 17: 4296–4308. doi: 10.1158/1078-0432.CCR-10-2557
    [8] Kmiecik J, Poli A, Brons NH, et al. (2013) Elevated CD3+ and CD8+ tumor-infiltrating immune cells correlate with prolonged survival in glioblastoma patients despite integrated immunosuppressive mechanisms in the tumor microenvironment and at the systemic level. J Neuroimmunol 264: 71–83. doi: 10.1016/j.jneuroim.2013.08.013
    [9] Yang I, Han SJ, Sughrue ME, et al. (2011a) Immune cell infiltrate differences in pilocytic astrocytoma and glioblastoma: evidence of distinct immunological microenvironments that reflect tumor biology. J Neurosurg 115: 505–511.
    [10] Swain SL (1995) T-cell subsets: Who does the polarizing? Curr Biol 5: 849–851. doi: 10.1016/S0960-9822(95)00170-9
    [11] Mellanby RJ, Thomas DC, Lamb J (2009) Role of regulatory T-cells in autoimmunity. Clin Sci 116: 639–469. doi: 10.1042/CS20080200
    [12] Fecci PE, Mitchell DA, Whitesides JF, et al. (2006) Increased regulatory T-cell fraction amidst a diminished CD4 compartment explains cellular immune defects in patients with malignant glioma. Cancer Res 66: 3294–3302. doi: 10.1158/0008-5472.CAN-05-3773
    [13] Fecci PE, Ochiai H, Mitchell DA, et al. (2007) Systemic CTLA-4 blockade ameliorates glioma-induced changes to the CD4+ T cell compartment without affecting regulatory T-cell function. Clin Cancer Res 13: 2158–2167. doi: 10.1158/1078-0432.CCR-06-2070
    [14] Thomas AA, Fisher JL, Rahme GJ, et al. (2015) Regulatory T cells are not a strong predictor of survival for patients with glioblastoma. Neuro Oncol 17: 801–809. doi: 10.1093/neuonc/nou363
    [15] Han S, Zhang C, Li Q, et al. (2014) Tumour-infiltrating CD4(+) and CD8(+) lymphocytes as predictors of clinical outcome in glioma. Brit J Cancer 110: 2560–2568. doi: 10.1038/bjc.2014.162
    [16] Sayour EJ, McLendon P, McLendon R, et al. (2015) Increased proportion of FoxP3+ regulatory T cells in tumor infiltrating lymphocytes is associated with tumor recurrence and reduced survival in patients with glioblastoma. Cancer Immunol Immun 64: 419–427. doi: 10.1007/s00262-014-1651-7
    [17] Mu L, Yang C, Gao Q, et al. (2017) CD4+ and perivascular Foxp3+ T cells in glioma correlate with angiogenesis and tumor progression. Front Immunol 8: 1451. doi: 10.3389/fimmu.2017.01451
    [18] Braumuller H, Wieder T, Brenner E, et al. (2013) T-helper-1-cell cytokines drive cancer into senescence. Nature 494: 361–365. doi: 10.1038/nature11824
    [19] Hirschhorn-Cymerman D, Budhu S, Kitano S, et al. (2012) Induction of tumoricidal function in CD4+ T cells is associated with concomitant memory and terminally differentiated phenotype. J Exp Med 209: 2113–2126. doi: 10.1084/jem.20120532
    [20] Perez-Diez A, Joncker NT, Choi K, et al. (2007) CD4 cells can be more efficient at tumor rejection than CD8 cells. Blood 109: 5346–5354. doi: 10.1182/blood-2006-10-051318
    [21] Murphy KA, Erickson JR, Johnson CS, et al. (2014) CD8+ T cell-independent tumor regression induced by Fc-OX40L and therapeutic vaccination in a mouse model of glioma. J Immunol 192: 224–233. doi: 10.4049/jimmunol.1301633
    [22] Saha D, Martuza RL, Rabkin SD (2017) Macrophage polarization contributes to glioblastoma eradication by combination immunovirotherapy and immune checkpoint blockade. Cancer Cell 32: 253–267. doi: 10.1016/j.ccell.2017.07.006
    [23] Liu Z, Meng Q, Bartek J, et al. (2017b) Tumor-infiltrating lymphocytes (TILs) from patients with glioma. Oncoimmunology 6: e1252894.
    [24] Beck BH, Kim H, O'Brien R, et al. (2015) Dynamics of circulating gammadelta T cell activity in an immunocompetent mouse model of high-grade glioma. PLoS One 10: e0122387. doi: 10.1371/journal.pone.0122387
    [25] Yang I, Tihan T, Han SJ, et al. (2010) CD8+ T-cell infiltrate in newly diagnosed glioblastoma is associated with long-term survival. J Clin Neurosci 17: 1381–1385. doi: 10.1016/j.jocn.2010.03.031
    [26] Nduom EK, Wei J, Yaghi NK, et al. (2016) PD-L1 expression and prognostic impact in glioblastoma. Neuro Oncol 18: 195–205. doi: 10.1093/neuonc/nov172
    [27] Heiland DH, Haaker G, Delev D, et al. (2017) Comprehensive analysis of PD-L1 expression in glioblastoma multiforme. Oncotarget 8: 42214–42225.
    [28] Reiss SN, Yerram P, Modelevsky L, et al. (2017) Retrospective review of safety and efficacy of programmed cell death-1 inhibitors in refractory high grade gliomas. J Immunother Cancer 5: 99. doi: 10.1186/s40425-017-0302-x
    [29] Miyauchi JT, Tsirka SE (2017) Advances in immunotherapeutic research for glioma therapy. J Neurol, 1–16.
    [30] Nakashima H, Alayo QA, Penaloza-MacMaster P, et al. (2018) Modeling tumor immunity of mouse glioblastoma by exhausted CD8+ T cells. Sci Rep 8: 208. doi: 10.1038/s41598-017-18540-2
    [31] Haanen J (2017) Converting cold into hot tumors by combining immunotherapies. Cell 170: 1055–1056. doi: 10.1016/j.cell.2017.08.031
    [32] Zeng J, See AP, Phallen J, et al. (2013) Anti-PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas. Int J Radiat Oncol 86: 343–349. doi: 10.1016/j.ijrobp.2012.12.025
    [33] Waitz R, Solomon SB, Petre EN, et al. (2012) Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy. Cancer Res 72: 430–439. doi: 10.1158/0008-5472.CAN-11-1782
    [34] Masson F, Calzascia T, Di BBW, et al. (2007) Brain microenvironment promotes the final functional maturation of tumor-specific effector CD8+ T cells. J Immunol 179: 845–853. doi: 10.4049/jimmunol.179.2.845
    [35] Hong JJ, Rosenberg SA, Dudley ME, et al. (2010) Successful treatment of melanoma brain metastases with adoptive cell therapy. Clin Cancer Res 16: 4892–4898. doi: 10.1158/1078-0432.CCR-10-1507
    [36] Rosenberg SA, Yang JC, Sherry RM, et al. (2011) Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 17: 4550–1557. doi: 10.1158/1078-0432.CCR-11-0116
    [37] Brown CE, Badie B, Barish ME, et al. (2015) Bioactivity and safety of IL13Ralpha2-redirected chimeric antigen receptor CD8+ T cells in patients with recurrent glioblastoma. Clin Cancer Res 21: 4062–4072. doi: 10.1158/1078-0432.CCR-15-0428
    [38] Brown CE, Alizadeh D, Starr R, et al. (2016) Regression of glioblastoma after chimeric antigen receptor T-cell therapy. New Engl J Med 375: 2561–2569. doi: 10.1056/NEJMoa1610497
    [39] Liau LM, Prins RM, Kiertscher SM, et al. (2005) Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res 11: 5515–5525. doi: 10.1158/1078-0432.CCR-05-0464
    [40] Polyzoidis S, Ashkan K (2014) DCVax(R)-L--developed by Northwest Biotherapeutics. Hum Vacc Immunother 10: 3139–3145. doi: 10.4161/hv.29276
    [41] Flores C, Pham C, Snyder D, et al. (2015) Novel role of hematopoietic stem cells in immunologic rejection of malignant gliomas. Oncoimmunology 4: e994374. doi: 10.4161/2162402X.2014.994374
    [42] Muller I, Altherr D, Eyrich M, et al. (2016) Tumor antigen-specific T cells for immune monitoring of dendritic cell-treated glioblastoma patients. Cytotherapy 18: 1146–1161. doi: 10.1016/j.jcyt.2016.05.014
    [43] Garg AD, Vandenberk L, Koks C, et al. (2016) Dendritic cell vaccines based on immunogenic cell death elicit danger signals and T cell-driven rejection of high-grade glioma. Sci Transl Med 8: 328ra27.
    [44] Mitchell DA, Batich KA, Gunn MD, et al. (2015) Tetanus toxoid and CCL3 improve dendritic cell vaccines in mice and glioblastoma patients. Nature 519: 366–369. doi: 10.1038/nature14320
    [45] Ransohoff RM (2016) A polarizing question: do M1 and M2 microglia exist? Nat Neurosci 19: 987–991. doi: 10.1038/nn.4338
    [46] Charles NA, Holland EC, Gilbertson R, et al. (2011) The brain tumor microenvironment. Glia 59: 1169–1180. doi: 10.1002/glia.21136
    [47] Da FA, Badie B (2013) Microglia and macrophages in malignant gliomas: recent discoveries and implications for promising therapies. Clin Dev Immunol 2013: 264124.
    [48] Hewedi IH, Radwan NA, Shash LS, et al. (2013) Perspectives on the immunologic microenvironment of astrocytomas. Cancer Manag Res 5: 293–299.
    [49] Held-Feindt J, Hattermann K, Muerkoster SS, et al. (2010) CX3CR1 promotes recruitment of human glioma-infiltrating microglia/macrophages (GIMs). Exp Cell Res 316: 1553–1566. doi: 10.1016/j.yexcr.2010.02.018
    [50] Nishie A, Ono M, Shono T, et al. (1999) Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clin Cancer Res 5: 1107–1113.
    [51] Sorensen MD, Dahlrot RH, Boldt HB, et al. (2017) Tumour-associated microglia/macrophages predict poor prognosis in high-grade gliomas and correlate with an aggressive tumour subtype. Neuropath Appl Neuro 44: 185–206.
    [52] Okada M, Saio M, Kito Y, et al. (2009) Tumor-associated macrophage/microglia infiltration in human gliomas is correlated with MCP-3, but not MCP-1. Int J Oncol 34: 1621–1627.
    [53] Wang Q, Hu B, Hu X, et al. (2017) Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell 32: 42–56. doi: 10.1016/j.ccell.2017.06.003
    [54] Bloch O, Crane CA, Kaur R, et al. (2013) Gliomas promote immunosuppression through induction of B7-H1 expression in tumor-associated macrophages. Clin Cancer Res 19: 3165–3175. doi: 10.1158/1078-0432.CCR-12-3314
    [55] Gieryng A, Pszczolkowska D, Bocian K, et al. (2017) Immune microenvironment of experimental rat C6 gliomas resembles human glioblastomas. Sci Rep 7: 17556. doi: 10.1038/s41598-017-17752-w
    [56] Xu S, Wei J, Wang F, et al. (2014) Effect of miR-142-3p on the M2 macrophage and therapeutic efficacy against murine glioblastoma. J Natl Cancer Inst 106.
    [57] McFarland BC, Marks MP, Rowse AL, et al. (2016) Loss of SOCS3 in myeloid cells prolongs survival in a syngeneic model of glioma. Oncotarget 7: 20621–20635.
    [58] Pyonteck SM, Akkari L, Schuhmacher AJ, et al. (2013) CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 19: 1264–1272. doi: 10.1038/nm.3337
    [59] Yan D, Kowal J, Akkari L, et al. (2017) Inhibition of colony stimulating factor-1 receptor abrogates microenvironment-mediated therapeutic resistance in gliomas. Oncogene 36: 6049–6058. doi: 10.1038/onc.2017.261
    [60] Colegio OR, Chu NQ, Szabo AL, et al. (2014) Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 513: 559–563. doi: 10.1038/nature13490
    [61] Zhang I, Alizadeh D, Liang J, et al. (2016) Characterization of arginase expression in glioma-associated microglia and macrophages. PLoS One 11: e0165118. doi: 10.1371/journal.pone.0165118
    [62] Lyons YA, Pradeep S, Wu SY, et al. (2017) Macrophage depletion through colony stimulating factor 1 receptor pathway blockade overcomes adaptive resistance to anti-VEGF therapy. Oncotarget 8: 96496–96505.
    [63] Nakayama T, Kurobe H, Sugasawa N, et al. (2013) Role of macrophage-derived hypoxia-inducible factor (HIF)-1alpha as a mediator of vascular remodelling. Cardiovasc Res 99: 705–715. doi: 10.1093/cvr/cvt146
    [64] Jetten N, Verbruggen S, Gijbels MJ, et al. (2014) Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 17: 109–118. doi: 10.1007/s10456-013-9381-6
    [65] Chang AL, Miska J, Wainwright DA, et al. (2016) CCL2 produced by the glioma microenvironment is essential for the recruitment of regulatory t cells and myeloid-derived suppressor cells. Cancer Res 76: 5671–5682. doi: 10.1158/0008-5472.CAN-16-0144
    [66] Solga AC, Pong WW, Kim KY, et al. (2015) RNA sequencing of tumor-associated microglia reveals Ccl5 as a stromal chemokine critical for neurofibromatosis-1 glioma growth. Neoplasia 17: 776–788. doi: 10.1016/j.neo.2015.10.002
    [67] Nissen JC, Selwood DL, Tsirka SE (2013) Tuftsin signals through its receptor neuropilin-1 via the transforming growth factor beta pathway. J Neurochem 127: 394–402. doi: 10.1111/jnc.12404
    [68] Miyauchi JT, Chen D, Choi M, et al. (2016) Ablation of neuropilin 1 from glioma-associated microglia and macrophages slows tumor progression. Oncotarget 7: 9801–9814.
    [69] Koncina E, Roth L, Gonthier B, et al. (2007) Role of semaphorins during axon growth and guidance. Adv Exp Med Biol 621: 50–64. doi: 10.1007/978-0-387-76715-4_4
    [70] Glinka Y, Prud'homme GJ (2008) Neuropilin-1 is a receptor for transforming growth factor beta-1, activates its latent form, and promotes regulatory T cell activity. J Leukoc Biol 84: 302–10. doi: 10.1189/jlb.0208090
    [71] Hu B, Guo P, Bar-Joseph I, et al. (2007) Neuropilin-1 promotes human glioma progression through potentiating the activity of the HGF/SF autocrine pathway. Oncogene 26: 5577–5586. doi: 10.1038/sj.onc.1210348
    [72] Gelfand MV, Hagan N, Tata A, et al. (2014) Neuropilin-1 functions as a VEGFR2 co-receptor to guide developmental angiogenesis independent of ligand binding. Elife 3: e03720.
    [73] Nakamura F, Goshima Y (2002) Structural and functional relation of neuropilins. Adv Exp Med Biol 515: 55–69. doi: 10.1007/978-1-4615-0119-0_5
    [74] Chaudhary B, Khaled YS, Ammori BJ, et al. (2014) Neuropilin 1: function and therapeutic potential in cancer. Cancer Immunol Immun 63: 81–99. doi: 10.1007/s00262-013-1500-0
    [75] Raimondi C, Fantin A, Lampropoulou A, et al. (2014) Imatinib inhibits VEGF-independent angiogenesis by targeting neuropilin 1-dependent ABL1 activation in endothelial cells. J Exp Med 211: 1167–1183. doi: 10.1084/jem.20132330
    [76] Campos-Mora M, Morales RA, Gajardo T, et al. (2013) Neuropilin-1 in transplantation tolerance. Front Immunol 4: 405.
    [77] Klagsbrun M, Takashima S, Mamluk R (2002) The role of neuropilin in vascular and tumor biology. Adv Exp Med Biol 515: 33–48. doi: 10.1007/978-1-4615-0119-0_3
    [78] Zachary I, Fantin A, Herzog B, et al. (2014) Neuropilin 1 (NRP1) hypomorphism combined with defective VEGF-A binding reveals novel roles for NRP1 in developmental and pathological angiogenesis. Development 141: 556–562. doi: 10.1242/dev.103028
    [79] Campos-Mora M, Morales RA, Perez F, et al. (2015) Neuropilin-1(+) regulatory T cells promote skin allograft survival and modulate effector CD4(+) T cells phenotypic signature. Immunol Cell Biol 93: 113–119. doi: 10.1038/icb.2014.77
    [80] Solomon BD, Mueller C, Chae WJ, et al. (2011) Neuropilin-1 attenuates autoreactivity in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 108: 2040–2045. doi: 10.1073/pnas.1008721108
    [81] Delgoffe GM, Woo SR, Turnis ME, et al. (2013) Stability and function of regulatory T cells is maintained by a neuropilin-1-semaphorin-4a axis. Nature 501: 252–256. doi: 10.1038/nature12428
    [82] Hansen W, Hutzler M, Abel S, et al. (2012) Neuropilin 1 deficiency on CD4+Foxp3+ regulatory T cells impairs mouse melanoma growth. J Exp Med 209: 2001–2016. doi: 10.1084/jem.20111497
    [83] Milpied P, Massot B, Renand A, et al. (2011) IL-17-producing invariant NKT cells in lymphoid organs are recent thymic emigrants identified by neuropilin-1 expression. Blood 118: 2993–3002. doi: 10.1182/blood-2011-01-329268
    [84] Sarris M, Andersen KG, Randow F, et al. (2008) Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity 28: 402–413. doi: 10.1016/j.immuni.2008.01.012
    [85] Bourbie-Vaudaine S, Blanchard N, Hivroz C, et al. (2006) Dendritic cells can turn CD4+ T lymphocytes into vascular endothelial growth factor-carrying cells by intercellular neuropilin-1 transfer. J Immunol 177: 1460–1469. doi: 10.4049/jimmunol.177.3.1460
    [86] Casazza A, Laoui D, Wenes M, et al. (2013) Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores antitumor immunity. Cancer Cell 24: 695–709. doi: 10.1016/j.ccr.2013.11.007
    [87] Dejda A, Mawambo G, Daudelin JF, et al. (2016) Neuropilin-1-expressing microglia are associated with nascent retinal vasculature yet dispensable for developmental angiogenesis. Invest Ophth Vis Sci 57: 1530–1536. doi: 10.1167/iovs.15-18598
    [88] Zhang W, Lv Y, Xue Y, et al. (2016b) Co-expression modules of NF1, PTEN and sprouty enable distinction of adult diffuse gliomas according to pathway activities of receptor tyrosine kinases. Oncotarget 7: 59098–59114.
    [89] Glinka Y, Stoilova S, Mohammed N, et al. (2011) Neuropilin-1 exerts co-receptor function for TGF-beta-1 on the membrane of cancer cells and enhances responses to both latent and active TGF-beta. Carcinogenesis 32: 613–621. doi: 10.1093/carcin/bgq281
    [90] Miyauchi JT, Caponegro MD, Chen D, et al. (2017) Deletion of neuropilin 1 from microglia or bone marrow-derived macrophages slows glioma progression. Cancer Res 78: 685–694.
    [91] Osada H, Tokunaga T, Nishi M, et al. (2004) Overexpression of the neuropilin 1 (NRP1) gene correlated with poor prognosis in human glioma. Anticancer Res 24: 547–552.
    [92] Chen L, Miao W, Tang X, et al. (2013) Inhibitory effect of neuropilin-1 monoclonal antibody (NRP-1 MAb) on glioma tumor in mice. J Biomed Nanotechnol 9: 551–558. doi: 10.1166/jbn.2013.1623
    [93] Formolo CA, Williams R, Gordish-Dressman H, et al. (2011) Secretome signature of invasive glioblastoma multiforme. J Proteome Res 10: 3149–3159. doi: 10.1021/pr200210w
    [94] Li X, Tang T, Lu X, et al. (2011) RNA interference targeting NRP-1 inhibits human glioma cell proliferation and enhances cell apoptosis. Mol Med Rep 4: 1261–1266.
    [95] Nasarre C, Roth M, Jacob L, et al. (2010) Peptide-based interference of the transmembrane domain of neuropilin-1 inhibits glioma growth in vivo. Oncogene 29: 2381–2392. doi: 10.1038/onc.2010.9
    [96] Bagci T, Wu JK, Pfannl R, et al. (2009) Autocrine semaphorin 3A signaling promotes glioblastoma dispersal. Oncogene 28: 3537–3550. doi: 10.1038/onc.2009.204
    [97] Treps L, Edmond S, Harford-Wright E, et al. (2016) Extracellular vesicle-transported Semaphorin3A promotes vascular permeability in glioblastoma. Oncogene 35: 2615–2623. doi: 10.1038/onc.2015.317
    [98] Jacob L, Sawma P, Garnier N, et al. (2016) Inhibition of PlexA1-mediated brain tumor growth and tumor-associated angiogenesis using a transmembrane domain targeting peptide. Oncotarget 7: 57851–57865.
    [99] Sulpice E, Plouet J, Berge M, et al. (2008) Neuropilin-1 and neuropilin-2 act as coreceptors, potentiating proangiogenic activity. Blood 111: 2036–2045. doi: 10.1182/blood-2007-04-084269
    [100] Hamerlik P, Lathia JD, Rasmussen R, et al. (2012) Autocrine VEGF-VEGFR2-Neuropilin-1 signaling promotes glioma stem-like cell viability and tumor growth. J Exp Med 209: 507–520. doi: 10.1084/jem.20111424
    [101] Gilbert MR, Dignam JJ, Armstrong TS, et al. (2014) A randomized trial of bevacizumab for newly diagnosed glioblastoma. New Engl J Med 370: 699–708. doi: 10.1056/NEJMoa1308573
    [102] Frei K, Gramatzki D, Tritschler I, et al. (2015) Transforming growth factor-beta pathway activity in glioblastoma. Oncotarget 6: 5963–5977.
    [103] Maxwell M, Galanopoulos T, Neville-Golden J, et al. (1992) Effect of the expression of transforming growth factor-beta 2 in primary human glioblastomas on immunosuppression and loss of immune surveillance. J Neurosurg 76: 799–804. doi: 10.3171/jns.1992.76.5.0799
    [104] Platten M, Wick W, Weller M (2001) Malignant glioma biology: role for TGF-beta in growth, motility, angiogenesis, and immune escape. Microsc Res Tech 52: 401–410. doi: 10.1002/1097-0029(20010215)52:4<401::AID-JEMT1025>3.0.CO;2-C
    [105] Chen ML, Pittet MJ, Gorelik L, et al. (2005) Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo. Proc Natl Acad Sci USA 102: 419–424. doi: 10.1073/pnas.0408197102
    [106] Thomas DA, Massague J (2005) TGF-beta directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 8: 369–380. doi: 10.1016/j.ccr.2005.10.012
    [107] Wesolowska A, Kwiatkowska A, Slomnicki L, et al. (2008) Microglia-derived TGF-beta as an important regulator of glioblastoma invasion--an inhibition of TGF-beta-dependent effects by shRNA against human TGF-beta type II receptor. Oncogene 27: 918–930. doi: 10.1038/sj.onc.1210683
    [108] Uhl M, Aulwurm S, Wischhusen J, et al. (2004) SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res 64: 7954–7961. doi: 10.1158/0008-5472.CAN-04-1013
    [109] Ueda R, Fujita M, Zhu X, et al. (2009) Systemic inhibition of transforming growth factor-beta in glioma-bearing mice improves the therapeutic efficacy of glioma-associated antigen peptide vaccines. Clin Cancer Res 15: 6551–6559. doi: 10.1158/1078-0432.CCR-09-1067
    [110] Rodon J, Carducci MA, Sepulveda-Sanchez JM, et al. (2015) First-in-human dose study of the novel transforming growth factor-beta receptor I kinase inhibitor LY2157299 monohydrate in patients with advanced cancer and glioma. Clin Cancer Res 21: 553–560. doi: 10.1158/1078-0432.CCR-14-1380
    [111] Falco SD (2012) The discovery of placenta growth factor and its biological activity. Exp Mol Med 44: 1–9. doi: 10.3858/emm.2012.44.1.025
    [112] Dewerchin M, Carmeliet P (2012) PlGF: a multitasking cytokine with disease-restricted activity. Csh Perspect Med 2: 143–152.
    [113] Lassen U, Chinot OL, McBain C, et al. (2015) Phase 1 dose-escalation study of the antiplacental growth factor monoclonal antibody RO5323441 combined with bevacizumab in patients with recurrent glioblastoma. Neuro Oncol 17: 1007–1015. doi: 10.1093/neuonc/nov019
    [114] Snuderl M, Batista A, Kirkpatrick ND, et al. (2013) Targeting placental growth factor/neuropilin 1 pathway inhibits growth and spread of medulloblastoma. Cell 152: 1065–1076. doi: 10.1016/j.cell.2013.01.036
    [115] Guo Y, Wang X, Tian X, et al. (2012) Tumor-derived hepatocyte growth factor is associated with poor prognosis of patients with glioma and influences the chemosensitivity of glioma cell line to cisplatin in vitro. World J Surg Oncol 10: 1–11. doi: 10.1186/1477-7819-10-1
    [116] Wen PY, Schiff D, Cloughesy TF, et al. (2011) A phase II study evaluating the efficacy and safety of AMG 102 (rilotumumab) in patients with recurrent glioblastoma. Neuro Oncol 13: 437–446. doi: 10.1093/neuonc/noq198
    [117] De Groot JF, Prados M, Urquhart T, et al. (2009) A phase II study of XL184 in patients (pts) with progressive glioblastoma multiforme (GBM) in first or second relapse. J Clin Oncol 27: 2047.
    [118] Schiff D, Desjardins A, Cloughesy T, et al. (2016) Phase 1 dose escalation trial of the safety and pharmacokinetics of cabozantinib concurrent with temozolomide and radiotherapy or temozolomide after radiotherapy in newly diagnosed patients with high-grade gliomas. Cancer 122: 582–587. doi: 10.1002/cncr.29798
    [119] Wu HB, Wang Z, Wang QS, et al. (2015) Use of labelled tLyP-1 as a novel ligand targeting the NRP receptor to image glioma. PLoS One 10: e0137676. doi: 10.1371/journal.pone.0137676
    [120] Ying M, Shen Q, Zhan C, et al. (2016) A stabilized peptide ligand for multifunctional glioma targeted drug delivery. J Control Release 243: 86–98. doi: 10.1016/j.jconrel.2016.09.035
    [121] Ying M, Zhan C, Wang S, et al. (2016) Liposome-based systemic glioma-targeted drug delivery enabled by all-d peptides. ACS Appl Mater Inter 8: 29977–29985. doi: 10.1021/acsami.6b10146
    [122] Liu C, Yao S, Li X, et al. (2017) iRGD-mediated core-shell nanoparticles loading carmustine and O6-benzylguanine for glioma therapy. J Drug Target 25: 235–246. doi: 10.1080/1061186X.2016.1238091
    [123] Liu Y, Mei L, Xu C, et al. (2016) Dual receptor recognizing cell penetrating peptide for selective targeting, efficient intratumoral diffusion and synthesized anti-glioma therapy. Theranostics 6: 177–191. doi: 10.7150/thno.13532
    [124] Bechet D, Auger F, Couleaud P, et al. (2015) Multifunctional ultrasmall nanoplatforms for vascular-targeted interstitial photodynamic therapy of brain tumors guided by real-time MRI. Nanomed-Nanotechnol 11: 657–670. doi: 10.1016/j.nano.2014.12.007
    [125] Patnaik A, Lorusso PM, Messersmith WA, et al. (2014) A Phase Ib study evaluating MNRP1685A, a fully human anti-NRP1 monoclonal antibody, in combination with bevacizumab and paclitaxel in patients with advanced solid tumors. Cancer Chemoth Pharm 73: 951–960. doi: 10.1007/s00280-014-2426-8
  • Reader Comments
  • © 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(4827) PDF downloads(972) Cited by(2)

Article outline

Figures and Tables

Figures(3)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog