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Review | Open Access

Emerging Role of Tumor-associated Macrophages as Therapeutic Targets in Glioblastoma Multiforme

Xian-Bin Lin1, Guo-Han Hu1( ), Hua-Lin Fu2, Wei-Lin Jin2,3( )
Department of Neurosurgery, Shanghai Changzheng Hospital, Second Military Medical University, Shanghai 200003, China
Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Bio-X Institutes, Ministry of Education; Institute of Nano Biomedicine and Engineering, Shanghai Jiao Tong University, Shanghai 200240, China
School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China
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Abstract

The most common types of primary brain tumors in adults are gliomas. Glioblastoma multiforme (GBM) is the most highly aggressive type of glioma. GBM contains various numbers of cells with characteristics of activated or dysmorphic macrophages/microglia. Among them, some cell types provide significant support for tumor growth, while others are able to inhibit tumor progression. These cells are generally considered part of the tumor stroma and are often described as TAMs (tumour-associated macrophages). The presence of TAMs has been linked to increased tumor grade and poor clinical outcome in GBM, suggesting that depletion or inhibition of these cells may suppress tumor growth. A better understanding of tumor microenvironment in the brain would therefore be expected to contribute to the development of improved therapies for brain tumors that are urgently required due to a poor availability of treatments for these malignancies. This review summarizes some of the known interactions between brain tumors and different stromal cells, and also discusses potential therapeutic approaches within this context.

Keywords

microenvironmentNanoprodrugimmunosuppressiveGBMTAMs

References

[1]

Kohanbash G, McKaveney K, Sakaki M, et al. GMCSF Promotes the Immunosuppressive Activity of Glioma-Infiltrating Myeloid Cells through Interleukin-4 Receptor-α. Cancer research, 2013, 73(21): 6413-6423.
Crossref Google Scholar
[2]

Okada H, Kohanbash G, Zhu X, et al. Immunotherapeutic approaches for glioma. Critical ReviewsTM in Immunology, 2009, 29(1): 1-42.
Crossref Google Scholar
[3]

Tran B, Rosenthal M A. Survival comparison between glioblastoma multiforme and other incurable cancers. Journal of Clinical Neuroscience, 2010, 17(4): 417-421.
Crossref Google Scholar
[4]

Goodenberger M K L, Jenkins R B. Genetics of adult glioma. Cancer genetics, 2012, 205(12): 613-621.
Crossref Google Scholar
[5]

Vredenburgh J J, Desjardins A, Reardon D A, et al. Experience with irinotecan for the treatment of malignant glioma. Neuro-oncology, 2009, 11(1): 80-91.
Crossref Google Scholar
[6]

Anton K, Baehring J M, Mayer T. Glioblastoma multiforme: overview of current treatment and future perspectives. Hematology/oncology clinics of North America, 2012, 26(4): 825-853.
Crossref Google Scholar
[7]

Stupp R, Hegi M E, Mason W P, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase Ⅲ study: 5-year analysis of the EORTC-NCIC trial. The lancet oncology, 2009, 10(5): 459-466.
Crossref Google Scholar
[8]

Poli A, Wang J, Domingues O, et al. Targeting glioblastoma with NK cells and mAb against NG2/CSPG4 prolongs animal survival. Oncotarget, 2013, 4(9): 1527.
Crossref Google Scholar
[9]

Ye X, Xu S, Xin Y, et al. Tumor-associated microglia/macrophages enhance the invasion of glioma stemlike cells via TGF-β1 signaling pathway. The Journal of Immunology, 2012, 189(1): 444-453.
Crossref Google Scholar
[10]

Zagzag D, Salnikow K, Chiriboga L, et al. Downregulation of major histocompatibility complex antigens in invading glioma cells: stealth invasion of the brain. Laboratory investigation, 2005, 85(3): 328-341.
Crossref Google Scholar
[11]

Hussain S F, Yang D, Suki D, et al. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro-oncology, 2006, 8(3): 261-279.
Crossref Google Scholar
[12]

Okada H, Kalinski P, Ueda R, et al. Induction of CD8+ T-cell responses against novel glioma–associated antigen peptides and clinical activity by vaccinations with α-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. Journal of Clinical Oncology, 2011, 29(3): 330-336.
Crossref Google Scholar
[13]

Pyonteck S M, Akkari L, Schuhmacher A J, et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nature medicine, 2013, 19(10): 1264-1272.
Crossref Google Scholar
[14]

Wen P Y, Kesari S. Malignant gliomas in adults. New England Journal of Medicine, 2008, 359(5): 492-507.
Crossref Google Scholar
[15]

Dunn G P, Rinne M L, Wykosky J, et al. Emerging insights into the molecular and cellular basis of glioblastoma. Genes & development, 2012, 26(8): 756-784.
Crossref Google Scholar
[16]
Balkwill F R, Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities.Seminars in cancer biology. Academic Press, 2012, 22(1): 33-40.
Crossref
[17]

Joyce J A, Pollard J W. Microenvironmental regulation of metastasis[J]. Nature Reviews Cancer, 2009, 9(4): 239-252.
Crossref Google Scholar
[18]

Põlajeva J, Bergström T, Edqvist P H, et al. Gliomaderived macrophage migration inhibitory factor (MIF) promotes mast cell recruitment in a STAT5-dependent manner. Molecular oncology, 2013, 8(1): 50-58.
Crossref Google Scholar
[19]

Hanahan D, Coussens L M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer cell, 2012, 21(3): 309-322.
Crossref Google Scholar
[20]

Arismendi-Morillo G, Castellano-Ramírez A, Medina Z. Ultrastructural characterization of macrophage-like mononuclear leukocytes in human astrocytic tumors. Ultrastructural pathology, 2010, 34(6): 321-326.
Crossref Google Scholar
[21]

Nyberg P, Salo T, Kalluri R. Tumor microenvironment and angiogenesis. Frontiers in bioscience: a journal and virtual library, 2007, 13: 6537-6553.
Crossref Google Scholar
[22]

Sasaki A, Yokoo H, Tanaka Y, et al. Characterization of microglia/macrophages in gliomas developed in S-100β-v-erbB transgenic rats. Neuropathology, 2013, 33(5): 505-514.
Crossref Google Scholar
[23]

Graeber M B, Streit W J. Microglia: biology and pathology. Acta neuropathologica, 2010, 119(1): 89-105.
Crossref Google Scholar
[24]

Garris C, Pittet M J. Therapeutically reeducating macrophages to treat GBM. Nature medicine, 2013, 19(10): 1207-1208.
Crossref Google Scholar
[25]

Wu A, Wei J, Kong L Y, et al. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro-oncology, 2010, 12(11): 1113-1125.
Crossref Google Scholar
[26]

Streit W J, Kreutzberg G W. Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. Journal of Comparative Neurology, 1988, 268(2): 248-263.
Crossref Google Scholar
[27]

Kostianovsky A M, Maier L M, Anderson R C, et al. Astrocytic regulation of human monocytic/microglial activation. The Journal of Immunology, 2008, 181(8): 5425-5432.
Crossref Google Scholar
[28]

van Rossum D, Hanisch U K. Microglia. Metabolic brain disease, 2004, 19(3-4): 393-411.
Crossref Google Scholar
[29]

Kennedy B C, Showers C R, Anderson D E, et al. Tumor-associated macrophages in glioma: friend or foe?. Journal of oncology, 2013, 2013:486912.
Crossref Google Scholar
[30]

MacMicking J, Xie Q, Nathan C. Nitric oxide and macrophage function. Annual review of immunology, 1997, 15(1): 323-350.
Crossref Google Scholar
[31]

Boehm U, Klamp T, Groot M, and Howard J C. Cellular responses to interferon-gamma. Annual Review of Immunology, 1997, 15:749-795,
Crossref Google Scholar
[32]

Hussain S F, Yang D, Suki D, et al. Innate immune functions of microglia isolated from human glioma patients. Journal of translational medicine, 2006, 4(1): 15.
Crossref Google Scholar
[33]

Sliwa M, Markovic D, Gabrusiewicz K, et al. The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain, 2007, 130(2): 476-489.
Crossref Google Scholar
[34]

Wesolowska A, Kwiatkowska A, Slomnicki L, et al. Microglia-derived TGF-β as an important regulator of glioblastoma invasion—an inhibition of TGF-β-dependent effects by shRNA against human TGF-β type Ⅱ receptor. Oncogene, 2008, 27(7): 918-930.
Crossref Google Scholar
[35]

Voronov E, Shouval D S, Krelin Y, et al. IL-1 is required for tumor invasiveness and angiogenesis. Proceedings of the National Academy of Sciences, 2003, 100(5): 2645-2650.
Crossref Google Scholar
[36]

Hiratsuka S, Nakamura K, Iwai S, et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer cell, 2002, 2(4): 289-300.
Crossref Google Scholar
[37]

Komohara Y, Ohnishi K, Kuratsu J, et al. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. The Journal of pathology, 2008, 216(1): 15-24.
Crossref Google Scholar
[38]

Wang S C, Hong J H, Hsueh C, et al. Tumor-secreted SDF-1 promotes glioma invasiveness and TAM tropism toward hypoxia in a murine astrocytoma model. Laboratory Investigation, 2012, 92(1): 151-162.
Crossref Google Scholar
[39]

Badie B, Schartner J M. Flow cytometric characterization of tumor-associated macrophages in experimental gliomas. Neurosurgery, 2000, 46(4): 957-962.
Crossref Google Scholar
[40]

Kennedy B C, Maier L M, D'Amico R, et al. Dynamics of central and peripheral immunomodulation in a murine glioma model. BMC immunology, 2009, 10(1): 11.
Crossref Google Scholar
[41]

Li W, Graeber M B. The molecular profile of microglia under the influence of glioma. Neuro-oncology, 2012, 14(8): 958-978.
Crossref Google Scholar
[42]

Filipazzi P, Huber V, Rivoltini L. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients. Cancer Immunology, Immunotherapy, 2012, 61(2): 255-263.
Crossref Google Scholar
[43]

Rodrigues J C, Gonzalez G C, Zhang L, et al. Normal human monocytes exposed to glioma cells acquire myeloid-derived suppressor cell-like properties. Neurooncology, 2010, 12(4): 351-365.
Crossref Google Scholar
[44]

Huettner C, Czub S, Kerkau S, et al. Interleukin 10 is expressed in human gliomas in vivo and increases glioma cell proliferation and motility in vitro. Anticancer research, 1996, 17(5A): 3217-3224.
Google Scholar
[45]

Badie B, Schartner J, Prabakaran S, et al. Expression of Fas ligand by microglia: possible role in glioma immune evasion. Journal of neuroimmunology, 2001, 120(1): 19-24.
Crossref Google Scholar
[46]

Didenko V V, Ngo H N, Minchew C, et al. Apoptosis of T lymphocytes invading glioblastomas multiforme: a possible tumor defense mechanism. Journal of neurosurgery, 2002, 96(3): 580.
Crossref Google Scholar
[47]

Ford A L, Foulcher E, Lemckert F A, et al. Microglia induce CD4 T lymphocyte final effector function and death. The Journal of experimental medicine, 1996, 184(5): 1737-1745.
Crossref Google Scholar
[48]

Jansen T, Tyler B, Mankowski J L, et al. FasL gene knock-down therapy enhances the antiglioma immune response. Neuro-oncology, 2010, 12(5): 482-489.
Google Scholar
[49]

Mitchell D A, Fecci P E, Sampson J H. Immunotherapy of malignant brain tumors. Immunological reviews, 2008, 222(1): 70-100.
Crossref Google Scholar
[50]

Wintterle S, Schreiner B, Mitsdoerffer M, et al. Expression of the B7-Related Molecule B7-H1 by Glioma Cells A Potential Mechanism of Immune Paralysis. Cancer research, 2003, 63(21): 7462-7467.
Google Scholar
[51]

Kjellman C, Olofsson S P, Hansson O, et al. Expression of TGF-β isoforms, TGF-β receptors, and SMAD molecules at different stages of human glioma. International Journal of Cancer, 2000, 89(3): 251-258.
Crossref Google Scholar
[52]

Germain D, Frank D A. Targeting the cytoplasmic and nuclear functions of signal transducers and activators of transcription 3 for cancer therapy. Clinical Cancer Research, 2007, 13(19): 5665-5669.
Crossref Google Scholar
[53]

Schartner J M, Hagar A R, Van Handel M, et al. Impaired capacity for upregulation of MHC class Ⅱ in tumor-associated microglia. Glia, 2005, 51(4): 279-285.
Crossref Google Scholar
[54]

Samuels V, Barrett J M, Bockman S, et al. Immunocytochemical study of transforming growth factor expression in benign and malignant gliomas. The American journal of pathology, 1989, 134(4): 894.
Google Scholar
[55]

Badie B, Schartner J, Klaver J, et al. In vitro modulation of microglia motility by glioma cells is mediated by hepatocyte growth factor/scatter factor. Neurosurgery, 1999, 44(5): 1077-1082.
Crossref Google Scholar
[56]

Tsai J C, Goldman C K, Gillespie G Y. Vascular endothelial growth factor in human glioma cell lines: induced secretion by EGF, PDGF-BB, and bFGF. Journal of neurosurgery, 1995, 82(5): 864-873.
Crossref Google Scholar
[57]

Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology, 2005, 69(Suppl. 3): 4-10.
Crossref Google Scholar
[58]

Shibuya M, Claesson-Welsh L. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Experimental cell research, 2006, 312(5): 549-560.
Crossref Google Scholar
[59]

Waltenberger J, Claesson-Welsh L, Siegbahn A, et al. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. Journal of Biological Chemistry, 1994, 269(43): 26988-26995.
Crossref Google Scholar
[60]

Alitalo K, Carmeliet P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer cell, 2002, 1(3): 219-227.
Crossref Google Scholar
[61]

Kerber M, Reiss Y, Wickersheim A, et al. Flt-1 signaling in macrophages promotes glioma growth in vivo. Cancer Research, 2008, 68(18): 7342-7351.
Crossref Google Scholar
[62]

Roggendorf W, Strupp S, Paulus W. Distribution and characterization of microglia/macrophages in human brain tumors. Acta neuropathologica, 1996, 92(3): 288-293.
Crossref Google Scholar
[63]

Hattori K, Dias S, Heissig B, et al. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. The Journal of experimental medicine, 2001, 193(9): 1005-1014.
Crossref Google Scholar
[64]

Murakami M, Iwai S, Hiratsuka S, et al. Signaling of vascular endothelial growth factor receptor-1 tyrosine kinase promotes rheumatoid arthritis through activation of monocytes/macrophages. Blood, 2006, 108(6): 1849-1856.
Crossref Google Scholar
[65]

Oura H, Bertoncini J, Velasco P, et al. A critical role of placental growth factor in the induction of inflammation and edema formation. Blood, 2003, 101(2): 560-567.
Crossref Google Scholar
[66]

Detmar M, Brown L F, Schön M P, et al. Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. Journal of Investigative Dermatology, 1998, 111(1): 1-6.
Crossref Google Scholar
[67]

Barbera-Guillem E, Nyhus J K, Wolford C C, et al. Vascular endothelial growth factor secretion by tumor-infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune complexes potentiate the process. Cancer research, 2002, 62(23): 7042-7049.
Google Scholar
[68]

Patel S, Player M R. Colony-stimulating factor-1 receptor inhibitors for the treatment of cancer and inflammatory disease. Current topics in medicinal chemistry, 2009, 9(7): 599-610.
Crossref Google Scholar
[69]

Ruffell B, Affara N I, Coussens L M. Differential macrophage programming in the tumor microenvironment. Trends in immunology, 2012, 33(3): 119-126.
Crossref Google Scholar
[70]

Bruna A, Darken R S, Rojo F, et al. High TGFβ-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer cell, 2007, 11(2): 147-160.
Crossref Google Scholar
[71]

Peñuelas S, Anido J, Prieto-Sánchez R M, et al. TGF-β increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer cell, 2009, 15(4): 315-327.
Crossref Google Scholar
[72]

Kim H S, Luo L, Pflugfelder S C, et al. Doxycycline inhibits TGF-β1–induced MMP-9 via Smad and MAPK pathways in human corneal epithelial cells. Investigative ophthalmology & visual science, 2005, 46(3): 840-848.
Crossref Google Scholar
[73]

Chen D, Ping Y, Yu S, et al. Downregulating FPR restrains xenograft tumors by impairing the angiogenic potential and invasive capability of malignant glioma cells. Biochemical and biophysical research communications, 2009, 381(3): 448-452.
Crossref Google Scholar
[74]

Massagué J. TGFβ in cancer. Cell, 2008, 134(2): 215-230.
Crossref Google Scholar
[75]

Bierie B, Moses H L. Transforming growth factor beta (TGF-β) and inflammation in cancer. Cytokine & growth factor reviews, 2010, 21(1): 49-59.
Crossref Google Scholar
[76]

Zhang Y E. Non-Smad pathways in TGF-β signaling. Cell research, 2009, 19(1): 128-139.
Crossref Google Scholar
[77]

Ikushima H, Todo T, Ino Y, et al. Autocrine TGF-β signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell stem cell, 2009, 5(5): 504-514.
Crossref Google Scholar
[78]

Yu S, Ping Y, Yi L, et al. Isolation and characterization of cancer stem cells from a human glioblastoma cell line U87. Cancer letters, 2008, 265(1): 124-134.
Crossref Google Scholar
[79]

Mantovani A, Schioppa T, Porta C, et al. Role of tumor-associated macrophages in tumor progression and invasion. Cancer and Metastasis Reviews, 2006, 25(3): 315-322.
Crossref Google Scholar
[80]

Shimato S, Anderson L M, Asslaber M, et al. Inhibition of Caveolin-1 Restores Myeloid Cell Function in Human Glioblastoma. PloS one, 2013, 8(10): e77397.
Crossref Google Scholar
[81]

Wang X M, Kim H P, Song R, et al. Caveolin-1 confers antiinflammatory effects in murine macrophages via the MKK3/p38 MAPK pathway. American journal of respiratory cell and molecular biology, 2006, 34(4): 434.
Crossref Google Scholar
[82]

Anderson R G. Caveolae: where incoming and outgoing messengers meet. Proceedings of the National Academy of Sciences, 1993, 90(23): 10909-10913.
Crossref Google Scholar
[83]

de Almeida C J, Witkiewicz A K, Jasmin J F, et al. Caveolin-2-deficient mice show increased sensitivity to endotoxemia. Cell Cycle, 2011, 10(13): 2151-2161.
Crossref Google Scholar
[84]

Harris J, Werling D, Hope J C, et al. Caveolae and caveolin in immune cells: distribution and functions. Trends in immunology, 2002, 23(3): 158-164.
Crossref Google Scholar
[85]

Santizo R A, Xu H L, Galea E, et al. Combined endothelial nitric oxide synthase upregulation and caveolin-1 downregulation decrease leukocyte adhesion in pial venules of ovariectomized female rats. Stroke, 2002, 33(2): 613-616.
Crossref Google Scholar
[86]

Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nature Reviews Immunology, 2007, 7(1): 41-51.
Crossref Google Scholar
[87]

Yoshimura A. Signal transduction of inflammatory cytokines and tumor development. Cancer science, 2006, 97(6): 439-447.
Crossref Google Scholar
[88]

Abou-Ghazal M, Yang D S, Qiao W, et al. The incidence, correlation with tumor-infiltrating inflammation, and prognosis of phosphorylated STAT3 expression in human gliomas. Clinical Cancer Research, 2008, 14(24): 8228-8235.
Crossref Google Scholar
[89]

Page B D G, Ball D P, Gunning P T. Signal transducer and activator of transcription 3 inhibitors: a patent review. Expert opinion on therapeutic patents, 2011, 21(1): 65-83.
Crossref Google Scholar
[90]

Cheng F, Wang H W, Cuenca A, et al. A critical role for Stat3 signaling in immune tolerance. Immunity, 2003, 19(3): 425-436.
Crossref Google Scholar
[91]

Wu L, Du H, Li Y, et al. Signal transducer and activator of transcription 3 (Stat3C) promotes myeloid-derived suppressor cell expansion and immune suppression during lung tumorigenesis. The American journal of pathology, 2011, 179(4): 2131-2141.
Crossref Google Scholar
[92]

Fujita M, Kohanbash G, Fellows-Mayle W, et al. COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer research, 2011, 71(7): 2664-2674.
Crossref Google Scholar
[93]

Hussain S F, Kong L Y, Jordan J, et al. A novel small molecule inhibitor of signal transducers and activators of transcription 3 reverses immune tolerance in malignant glioma patients. Cancer research, 2007, 67(20): 9630-9636.
Crossref Google Scholar
[94]

Komohara Y, Horlad H, Ohnishi K, et al. Importance of direct macrophage - Tumor cell interaction on progression of human glioma. Cancer science, 2012, 103(12): 2165-2172.
Crossref Google Scholar
[95]

Komohara Y, Horlad H, Ohnishi K, et al. M2 macrophage/microglial cells induce activation of Stat3 in primary central nervous system lymphoma. J Clin Exp Hematop, 2011, 51(2): 93-99.
Crossref Google Scholar
[96]
Balkwill F. Chemokine biology in cancer. Seminars in immunology. Academic Press, 2003, 15(1): 49-55.
Crossref
[97]

Dewan M Z, Ahmed S, Iwasaki Y, et al. Stromal cell-derived factor-1 and CXCR4 receptor interaction in tumor growth and metastasis of breast cancer. Biomedicine & pharmacotherapy, 2006, 60(6): 273-276.
Crossref Google Scholar
[98]

Aghi M, Cohen K S, Klein R J, et al. Tumor stromal-derived factor-1 recruits vascular progenitors to mitotic neovasculature, where microenvironment influences their differentiated phenotypes. Cancer research, 2006, 66(18): 9054-9064.
Crossref Google Scholar
[99]
Bazan J F, Bacon K B, Hardiman G, et al. A new class of membrane-bound chemokine with a CX3C motif[J]. 1997, 385(6617): 640-4.
Crossref
[100]

Held-Feindt J, Hattermann K, Müerköster S S, et al. CX3CR1 promotes recruitment of human glioma-infiltrating microglia/macrophages (GIMs). Experimental cell research, 2010, 316(9): 1553-1566.
Crossref Google Scholar
[101]

Imai T, Hieshima K, Haskell C, et al. Identification and Molecular Characterization of Fractalkine Receptor CX3CR1, which Mediates Both Leukocyte Migration and Adhesion. Cell, 1997, 91(4): 521-530.
Crossref Google Scholar
[102]

Rodero M, Marie Y, Coudert M, et al. Polymorphism in the microglial cell-mobilizing CX3CR1 gene is associated with survival in patients with glioblastoma. Journal of Clinical Oncology, 2008, 26(36): 5957-5964.
Crossref Google Scholar
[103]

Xin H, Kikuchi T, Andarini S, et al. Antitumor immune response by CX3CL1 fractalkine gene transfer depends on both NK and T cells. European journal of immunology, 2005, 35(5): 1371-1380.
Crossref Google Scholar
[104]
Somasundaram R, Herlyn D. Chemokines and the microenvironment in neuroectodermal tumor–host interaction. Seminars in cancer biology. Academic Press, 2009, 19(2): 92-96.
Crossref
[105]

Yu Y R A, Fong A M, Combadiere C, et al. Defective antitumor responses in CX3CR1 - deficient mice. International journal of cancer, 2007, 121(2): 316-322.
Crossref Google Scholar
[106]

Wang X, Tian X, Li Y, et al. Elevated expression of macrophage migration inhibitory factor correlates with tumor recurrence and poor prognosis of patients with gliomas. Journal of neuro-oncology, 2012, 106(1): 43-51.
Crossref Google Scholar
[107]

Conroy H, Mawhinney L, Donnelly S C. Inflammation and cancer: macrophage migration inhibitory factor (MIF) — the potential missing link. QJM, 2010, 103(11): 831-836.
Crossref Google Scholar
[108]

Cheng Y, Morshed R A, Auffinger B, et al. Multifunctional nanoparticles for brain tumor imaging and therapy. Advanced drug delivery reviews, 2014, 66C: 42-57.
Crossref Google Scholar
[109]

Groothuis D R. The blood-brain and blood-tumor barriers: a review of strategies for increasing drug delivery. Neuro-oncology, 2000, 2(1): 45-59.
Crossref Google Scholar
[110]

Begley D J, Brightman M W. Structural and functional aspects of the blood-brain barrier. Peptide transport and delivery into the central nervous system. Birkhäuser Basel, 2003: 39-78.
Crossref Google Scholar
[111]

Lee B S, Yoon C W, Osipov A, et al. Nanoprodrugs of NSAIDs: Preparation and characterization of flufenamic acid nanoprodrugs. Journal of drug delivery, 2011, 2011: 980720.
Crossref Google Scholar
[112]

Nduom E K, Bouras A, Kaluzova M, et al. Nanotechnology applications for glioblastoma. Neurosurgery Clinics of North America, 2012, 23(3): 439-449.
Crossref Google Scholar
[113]

Sarkar S, Döring A, Zemp F J, et al. Therapeutic activation of macrophages and microglia to suppress brain tumor-initiating cells. Nature neuroscience, 2014, 17(1): 46-55.
Crossref Google Scholar
[114]

Pallasch C P, Leskov I, Braun C J, et al. Sensitizing Protective Tumor Microenvironments to AntibodyMediated Therapy. Cell, 2014, 156(3): 590-602.
Crossref Google Scholar
Nano Biomedicine and Engineering
Volume 6 Issue 1,
March 2014
Pages 7-18
DOI: 10.5101/nbe.v6i1.p7-18
Cite this article:
Lin X-B, Hu G-H, Fu H-L, et al. Emerging Role of Tumor-associated Macrophages as Therapeutic Targets in Glioblastoma Multiforme. Nano Biomedicine and Engineering, 2014, 6(1): 7-18. https://doi.org/10.5101/nbe.v6i1.p7-18

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Received: 03 March 2014
Accepted: 18 March 2014
Published: 20 March 2014
© 2014 Xian-Bin Lin, Guo-Han Hu, Hua-Lin Fu and Wei-Lin Jin.

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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