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Original Research

Hypoxia induces macrophage polarization and re-education toward an M2 phenotype in U87 and U251 glioblastoma models

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Article: e1056442 | Received 13 Mar 2015, Accepted 24 May 2015, Published online: 17 Dec 2015

References

  • Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, Belanger K, Brandes AA, Marosi C, Bogdahn U et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352:987-96; PMID:15758009; http://dx.doi.org/10.1056/NEJMoa043330
  • Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H. The brain tumor microenvironment. Glia 2011; 59:1169-80; PMID:21446047; http://dx.doi.org/10.1002/glia.21136
  • Clavreul A, Etcheverry A, Chassevent A, Quillien V, Avril T, Jourdan M-L, Michalak S, François P, Carré J-L, Mosser J et al. Isolation of a new cell population in the glioblastoma microenvironment. J Neurooncol 2012; 106:493-504; PMID:21928115; http://dx.doi.org/10.1007/s11060-011-0701-7
  • Hirata K, Terasaka S, Shiga T, Hattori N, Magota K, Kobayashi H, Yamaguchi S, Houkin K, Tanaka S, Kuge Y et al. 18F-Fluoromisonidazole positron emission tomography may differentiate glioblastoma multiforme from less malignant gliomas. Eur J Nucl Med Mol Imaging 2012; 39:760-70; PMID:22307533; http://dx.doi.org/10.1007/s00259-011-2037-0
  • Rampling R, Cruickshank G, Lewis AD, Fitzsimmons SA, Workman P. Direct measurement of pO2 distribution and bioreductive enzymes in human malignant brain tumors. Int J Radiat Oncol Biol Phys 1994; 29:427-31; PMID:8005794; http://dx.doi.org/10.1016/0360-3016(94)90432-4
  • Evans SM, Judy KD, Dunphy I, Jenkins WT, Hwang W, Nelson PT, Lustig RA, Jenkins K, Magarelli DP, Hahn SM et al. Hypoxia is important in the biology and aggression of human glial brain tumors. Clin Cancer Res 2004; 10:8177-84; PMID:15623592; http://dx.doi.org/10.1158/1078-0432.CCR-04-1081
  • Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol 2005; 7:134-53; PMID:15831232; http://dx.doi.org/10.1215/S1152851704001115
  • Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 2007; 26:225-39; PMID:17440684; http://dx.doi.org/10.1007/s10555-007-9055-1
  • Spence AM, Muzi M, Swanson KR, O'Sullivan F, Rockhill JK, Rajendran JG, Adamsen TCH, Link JM, Swanson PE, Yagle KJ et al. Regional hypoxia in glioblastoma multiforme quantified with ; [18F]Fluoromisonidazole positron emission tomography before radiotherapy: correlation with time to progression and survival. Clin Cancer Res 2008; 14:2623-30; PMID:18451225; http://dx.doi.org/10.1158/1078-0432.CCR-07-4995
  • Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res 2006; 66:605-12; PMID:16423985; http://dx.doi.org/10.1158/0008-5472.CAN-05-4005
  • Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR, Liu K, Pamer EG, Li MO. The cellular and molecular origin of tumor-associated macrophages. Science 2014; 344:921-5; PMID:24812208; http://dx.doi.org/10.1126/science.1252510
  • Murdoch C, Giannoudis A, Lewis CE. Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood 2004; 104:2224-34; PMID:15231578; http://dx.doi.org/10.1182/blood-2004-03-1109
  • Badie B, Schartner JM. Flow cytometric characterization of tumor-associated macrophages in experimental gliomas. Neurosurgery 2000; 46:957-62; PMID:10764271; http://dx.doi.org/10.1097/00006123-200004000-00035
  • Strik HM, Stoll M, Meyermann R. Immune cell infiltration of intrinsic and metastatic intracranial tumours. Anticancer Res 2004; 24:37-42; PMID:15015573
  • Hussain SF, Yang D, Suki D, Aldape K, Grimm E, Heimberger AB. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro Oncol 2006; 8:261-79; PMID:16775224; http://dx.doi.org/10.1215/15228517-2006-008
  • Lu-Emerson C, Snuderl M, Kirkpatrick ND, Goveia J, Davidson C, Huang Y, Riedemann L, Taylor J, Ivy P, Duda DG et al. Increase in tumor-associated macrophages after antiangiogenic therapy is associated with poor survival among patients with recurrent glioblastoma. Neuro Oncol 2013; 15:1079-87; PMID:23828240; http://dx.doi.org/10.1093/neuonc/not082
  • Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002; 23:549-55; PMID:12401408; http://dx.doi.org/10.1016/S1471-4906(02)02302-5
  • Chang CI, Liao JC, Kuo L. Macrophage arginase promotes tumor cell growth and suppresses nitric oxide-mediated tumor cytotoxicity. Cancer Res 2001; 61:1100-6; PMID:11221839
  • Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122:787-95; PMID:22378047; http://dx.doi.org/10.1172/JCI59643
  • Biswas SK, Chittezhath M, Shalova IN, Lim J-Y. Macrophage polarization and plasticity in health and disease. Immunol Res 2012; 53:11-24; PMID:22418728; http://dx.doi.org/10.1007/s12026-012-8291-9
  • Biswas SK, Sica A, Lewis CE. Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms. J Immunol 2008; 180:2011-7; PMID:18250403; http://dx.doi.org/10.4049/jimmunol.180.4.2011
  • Huang Y, Snuderl M, Jain RK. Polarization of tumor-associated macrophages: a novel strategy for vascular normalization and antitumor immunity. Cancer Cell 2011; 19:1-2; PMID:21251607; http://dx.doi.org/10.1016/j.ccr.2011.01.005
  • Prosniak M, Harshyne LA, Andrews DW, Kenyon LC, Bedelbaeva K, Apanasovich TV, Heber-Katz E, Curtis MT, Cotzia P, Hooper DC. Glioma grade is associated with the accumulation and activity of cells bearing M2 monocyte markers. Clin Cancer Res 2013; 19:3776-86; PMID:23741072; http://dx.doi.org/10.1158/1078-0432.CCR-12-1940
  • Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 2013; 19:1264-72; PMID:24056773; http://dx.doi.org/10.1038/nm.3337
  • Lewis C, Murdoch C. Macrophage responses to hypoxia: implications for tumor progression and anti-cancer therapies. Am J Pathol 2005; 167:627-35; PMID:16127144; http://dx.doi.org/10.1016/S0002-9440(10)62038-X
  • Laoui D, Van Overmeire E, Di Conza G, Aldeni C, Keirsse J, Morias Y, Movahedi K, Houbracken I, Schouppe E, Elkrim Y et al. Tumor hypoxia does not drive differentiation of tumor-associated macrophages but rather fine-tunes the M2-like macrophage population. Cancer Res 2014; 74:24-30; PMID:24220244; http://dx.doi.org/10.1158/0008-5472.CAN-13-1196
  • Zhang J, Cao J, Ma S, Dong R, Meng W, Ying M, Weng Q, Chen Z, Ma J, Fang Q et al. Tumor hypoxia enhances non-small cell lung cancer metastasis by selectively promoting macrophage M2 polarization through the activation of ERK signaling. Oncotarget 2014;5:9664-77; PMID:25313135
  • Tafani M, Di Vito M, Frati A, Pellegrini L, De Santis E, Sette G, Eramo A, Sale P, Mari E, Santoro A et al. Pro-inflammatory gene expression in solid glioblastoma microenvironment and in hypoxic stem cells from human glioblastoma. J Neuroinflammation 2011; 8:32; PMID:21489226; http://dx.doi.org/10.1186/1742-2094-8-32
  • Tripathi C, Tewari BN, Kanchan RK, Baghel KS, Nautiyal N, Shrivastava R, Kaur H, Bhatt MLB, Bhadauria S. Macrophages are recruited to hypoxic tumor areas and acquire a pro-angiogenic M2-polarized phenotype via hypoxic cancer cell derived cytokines Oncostatin M and Eotaxin. Oncotarget 2014; 5:5350-68; PMID:25051364
  • Colegio OR, Chu N-Q, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 2014; 513:559-63; PMID:25043024; http://dx.doi.org/10.1038/nature13490
  • Takeda N, O'Dea EL, Doedens A, Kim J, Weidemann A, Stockmann C, Asagiri M, Simon MC, Hoffmann A, Johnson RS. Differential activation and antagonistic function of HIF-α isoforms in macrophages are essential for NO homeostasis. Genes Dev 2010; 24:491-501; PMID:20194441; http://dx.doi.org/10.1101/gad.1881410
  • Corroyer-Dulmont A, Pérès EA, Petit E, Durand L, Marteau L, Toutain J, Divoux D, Roussel S, MacKenzie ET, Barré L et al. Noninvasive assessment of hypoxia with 3-; [18F]-fluoro-1-(2-nitro-1-imidazolyl)-2-propanol (; [18F]-FMISO): a PET study in two experimental models of human glioma. Biol Chem 2013; 394:529-39; PMID:23399636; http://dx.doi.org/10.1515/hsz-2012-0318
  • Hou H, Krishnamurthy Nemani V, Du G, Montano R, Song R, Gimi B, Swartz HM, Eastman A, Khan N. Monitoring oxygen levels in orthotopic human glioma xenograft following carbogen inhalation and chemotherapy by implantable resonator-based oximetry. Int J Cancer 2014; 136:1688-96; PMID:25111969; http://dx.doi.org/10.1002/ijc.29132
  • Guillemin GJ, Brew BJ. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol 2004; 75:388-97; PMID:14612429; http://dx.doi.org/10.1189/jlb.0303114
  • Rempel SA, Dudas S, Ge S, Gutiérrez JA. Identification and localization of the cytokine SDF1 and its receptor, CXC chemokine receptor 4, to regions of necrosis and angiogenesis in human glioblastoma. Clin Cancer Res 2000; 6:102-11; PMID:10656438
  • Zagzag D, Esencay M, Mendez O, Yee H, Smirnova I, Huang Y, Chiriboga L, Lukyanov E, Liu M, Newcomb EW. Hypoxia- and vascular endothelial growth factor-induced stromal cell-derived factor-1α/CXCR4 expression in glioblastomas: one plausible explanation of scherer's structures. Am J Pathol 2008; 173:545-60; PMID:18599607; http://dx.doi.org/10.2353/ajpath.2008.071197
  • Pelegrin P, Surprenant A. Dynamics of macrophage polarization reveal new mechanism to inhibit IL-1beta release through pyrophosphates. EMBO J 2009; 28:2114-27; PMID:19536133; http://dx.doi.org/10.1038/emboj.2009.163
  • Murat A, Migliavacca E, Hussain SF, Heimberger AB, Desbaillets I, Hamou M-F, Rüegg C, Stupp R, Delorenzi M, Hegi ME. Modulation of angiogenic and inflammatory response in glioblastoma by hypoxia. PLoS One 2009; 4:e5947; PMID:19536297; http://dx.doi.org/10.1371/journal.pone.0005947
  • Chiang C-S, Fu SY, Wang S-C, Yu C-F, Chen F-H, Lin C-M, Hong J-H. Irradiation promotes an M2 macrophage phenotype in tumor hypoxia. Front Oncol 2012; 2:89; PMID:22888475; http://dx.doi.org/10.3389/fonc.2012.00089
  • Komohara Y, Ohnishi K, Kuratsu J, Takeya M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J Pathol 2008; 216:15-24; PMID:18553315; http://dx.doi.org/10.1002/path.2370
  • Movahedi K, Laoui D, Gysemans C, Baeten M, Stangé G, Van den Bossche J, Mack M, Pipeleers D, In't Veld P, De Baetselier P et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 2010; 70:5728-39; PMID:20570887; http://dx.doi.org/10.1158/0008-5472.CAN-09-4672
  • Leek RD, Talks KL, Pezzella F, Turley H, Campo L, Brown NS, Bicknell R, Taylor M, Gatter KC, Harris AL. Relation of hypoxia-inducible factor-2α (HIF-2α) expression in tumor-infiltrative macrophages to tumor angiogenesis and the oxidative thymidine phosphorylase pathway in human breast cancer. Cancer Res 2002; 62:1326-9; PMID:11888900
  • Burke B, Giannoudis A, Corke KP, Gill D, Wells M, Ziegler-Heitbrock L, Lewis CE. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol 2003; 163:1233-43; PMID:14507633; http://dx.doi.org/10.1016/S0002-9440(10)63483-9
  • Fang H-Y, Hughes R, Murdoch C, Coffelt SB, Biswas SK, Harris AL, Johnson RS, Imityaz HZ, Simon MC, Fredlund E et al. Hypoxia-inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia. Blood 2009; 114:844-59; PMID:19454749; http://dx.doi.org/10.1182/blood-2008-12-195941
  • Doedens AL, Stockmann C, Rubinstein MP, Liao D, Zhang N, DeNardo DG, Coussens LM, Karin M, Goldrath AW, Johnson RS. Macrophage expression of HIF-1α suppresses T cell function and promotes tumor progression. Cancer Res 2010; 70:7465-75; PMID:20841473; http://dx.doi.org/10.1158/0008-5472.CAN-10-1439
  • Koh MY, Powis G. Passing the baton: the HIF switch. Trends Biochem Sci 2012; 37:364-72; PMID:22818162; http://dx.doi.org/10.1016/j.tibs.2012.06.004
  • Sonveaux P, Végran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, De Saedeleer CJ, Kennedy KM, Diepart C, Jordan BF et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 2008; 118:3930-42; PMID:19033663; http://dx.doi.org/10.1172/JCI36843
  • Miranda-Gonçalves V, Honavar M, Pinheiro C, Martinho O, Pires MM, Pinheiro C, Cordeiro M, Bebiano G, Costa P, Palmeirim I et al. Monocarboxylate transporters (MCTs) in gliomas: expression and exploitation as therapeutic targets. Neuro Oncol 2013; 15:172-88; PMID:23258846; http://dx.doi.org/10.1093/neuonc/nos298
  • Stout RD, Jiang C, Matta B, Tietzel I, Watkins SK, Suttles J. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J Immunol 2005; 175:342-9; PMID:15972667; http://dx.doi.org/10.4049/jimmunol.175.1.342
  • Dehne N, Tausendschön M, Essler S, Geis T, Schmid T, Brüne B. IL-4 reduces the proangiogenic capacity of macrophages by down-regulating HIF-1α translation. J Leukoc Biol 2014; 95:129-37; PMID:24006507; http://dx.doi.org/10.1189/jlb.0113045
  • Goodman JE, Hofseth LJ, Hussain SP, Harris CC. Nitric oxide and p53 in cancer-prone chronic inflammation and oxyradical overload disease. Environ Mol Mutagen 2004; 44:3-9; PMID:15199542; http://dx.doi.org/10.1002/em.20024
  • Weigert A, Brüne B. Nitric oxide, apoptosis and macrophage polarization during tumor progression. Nitric Oxide 2008; 19:95-102; PMID:18486631; http://dx.doi.org/10.1016/j.niox.2008.04.021
  • Singh S, Gupta AK. Nitric oxide: role in tumour biology and iNOS/NO-based anticancer therapies. Cancer Chemother Pharmacol 2011; 67:1211-24; PMID:21544630; http://dx.doi.org/10.1007/s00280-011-1654-4
  • Hagemann T, Lawrence T, McNeish I, Charles KA, Kulbe H, Thompson RG, Robinson SC, Balkwill FR. “Re-educating” tumor-associated macrophages by targeting NF-kappaB. J Exp Med 2008; 205:1261-8; PMID:18490490; http://dx.doi.org/10.1084/jem.20080108
  • Buhtoiarov IN, Sondel PM, Wigginton JM, Buhtoiarova TN, Yanke EM, Mahvi DA, Rakhmilevich AL. Anti-tumour synergy of cytotoxic chemotherapy and anti-CD40 plus CpG-ODN immunotherapy through repolarization of tumour-associated macrophages. Immunology 2011; 132:226-39; PMID:21039467; http://dx.doi.org/10.1111/j.1365-2567.2010.03357.x
  • Garris C, Pittet MJ. Therapeutically reeducating macrophages to treat GBM. Nat Med 2013; 19:1207-8; PMID:24100977; http://dx.doi.org/10.1038/nm.3355
  • Huang Y, Yuan J, Righi E, Kamoun WS, Ancukiewicz M, Nezivar J, Santosuosso M, Martin JD, Martin MR, Vianello F et al. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci U S A 2012; 109:17561-6; PMID:23045683; http://dx.doi.org/10.1073/pnas.1215397109
  • Klug F, Prakash H, Huber PE, Seibel T, Bender N, Halama N, Pfirschke C, Voss RH, Timke C, Umansky L et al. Low-dose irradiation programs macrophage differentiation to an iNOS+/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 2013; 24:589-602; PMID:24209604; http://dx.doi.org/10.1016/j.ccr.2013.09.014
  • Stuhr LEB, Raa A, Oyan AM, Kalland KH, Sakariassen PO, Petersen K, Bjerkvig R, Reed RK. Hyperoxia retards growth and induces apoptosis, changes in vascular density and gene expression in transplanted gliomas in nude rats. J Neurooncol 2007; 85:191-202; PMID:17557137; http://dx.doi.org/10.1007/s11060-007-9407-2
  • Reiner NE, editor. Macrophages and Dendritic Cells: Methods and Protocols. New York, NY: Humana Press; 2009.