Macrophage Ablation Reduces M2-Like Populations and Jeopardizes Tumor Growth in a MAFIA-Based Glioma Model

Neoplasia (United States)

Volumn 17, Issue 4, 2015, Pages 374-384

  Gabrusiewicz, Konrad ^a   Hossain, Mohammad B ^a   Cortes Santiago, Nahir ^a   Fan, Xuejun ^a   Kaminska, Bozena ^b   Marini, Frank C ^c   Fueyo, Juan ^a   Gomez Manzano, Candelaria ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; AP 20187; COLONY STIMULATING FACTOR 1 RECEPTOR; COLONY STIMULATING FACTOR RECEPTOR; ENHANCED GREEN FLUORESCENT PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; FAS ANTIGEN; FAS PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER STAGING; CAPILLARY DENSITY; CELL DIFFERENTIATION; CONTROLLED STUDY; DIMERIZATION; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; GLIOMA; GLIOMA CELL LINE; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MICROGLIA; MITOSIS INDEX; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAW 264.7 CELL LINE; TRANSGENIC MOUSE; TUMOR ABLATION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANIMAL; BRAIN TUMOR; C57BL MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; BRAIN NEOPLASMS; CELL LINE, TUMOR; GLIOMA; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MONOCYTES;

EID: 84983484178     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2015.03.003     Document Type: Article

References (36)

1. [1] Hanahan, D, Weinberg, RA, Hallmarks of cancer: the next generation. Cell 144 (2011), 646–674.
2. [2] Charles, NA, Holland, EC, Gilbertson, R, Glass, R, Kettenmann, H, The brain tumor microenvironment. Glia 60 (2012), 502–514.
3. [3] Qian, BZ, Pollard, JW, Macrophage diversity enhances tumor progression and metastasis. Cell 141 (2010), 39–51.
4. [4] Bingle, L, Brown, NJ, Lewis, CE, The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 196 (2002), 254–265.
5. [5] Heusinkveld, M, van der Burg, SH, Identification and manipulation of tumor associated macrophages in human cancers. J Transl Med, 9, 2011, 216.
6. [6] Nishie, A, Ono, M, Shono, T, Fukushi, J, Otsubo, M, Onoue, H, Ito, Y, Inamura, T, Ikezaki, K, Fukui, M, et al. Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clin Cancer Res 5 (1999), 1107–1113.
7. [7] Rossi, ML, Jones, NR, Candy, E, Nicoll, JA, Compton, JS, Hughes, JT, Esiri, MM, Moss, TH, Cruz-Sanchez, FF, Coakham, HB, The mononuclear cell infiltrate compared with survival in high-grade astrocytomas. Acta Neuropathol 78 (1989), 189–193.
8. [8] Galarneau, H, Villeneuve, J, Gowing, G, Julien, JP, Vallieres, L, Increased glioma growth in mice depleted of macrophages. Cancer Res 67 (2007), 8874–8881.
9. [9] Zhai, H, Heppner, FL, Tsirka, SE, Microglia/macrophages promote glioma progression. Glia 59 (2011), 472–485.
10. [10] Burnett, SH, Kershen, EJ, Zhang, J, Zeng, L, Straley, SC, Kaplan, AM, Cohen, DA, Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J Leukoc Biol 75 (2004), 612–623.
11. [11] Winkler, IG, Sims, NA, Pettit, AR, Barbier, V, Nowlan, B, Helwani, F, Poulton, IJ, van Rooijen, N, Alexander, KA, Raggatt, LJ, et al. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116 (2010), 4815–4828.
12. [12] Chang, MK, Raggatt, LJ, Alexander, KA, Kuliwaba, JS, Fazzalari, NL, Schroder, K, Maylin, ER, Ripoll, VM, Hume, DA, Pettit, AR, Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol 181 (2008), 1232–1244.
13. [13] Alexander, KA, Chang, MK, Maylin, ER, Kohler, T, Muller, R, Wu, AC, Van Rooijen, N, Sweet, MJ, Hume, DA, Raggatt, LJ, et al. Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J Bone Miner Res 26 (2011), 1517–1532.
14. [14] Steel, CD, Kim, WK, Sanford, LD, Wellman, LL, Burnett, S, Van Rooijen, N, Ciavarra, RP, Distinct macrophage subpopulations regulate viral encephalitis but not viral clearance in the CNS. J Neuroimmunol 226 (2010), 81–92.
15. [15] Sun, Y, Karmakar, M, Roy, S, Ramadan, RT., Williams, SR, Howell, S, Shive, CL, Han, Y, Stopford, CM, Rietsch, A, et al. TLR4 and TLR5 on corneal macrophages regulate Pseudomonas aeruginosa keratitis by signaling through MyD88-dependent and -independent pathways. J Immunol 185 (2010), 4272–4283.
16. [16] Sasmono, RT, Oceandy, D, Pollard, JW, Tong, W, Pavli, P, Wainwright, BJ, Ostrowski, MC, Himes, SR, Hume, DA, A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101 (2003), 1155–1163.
17. [17] Cecchini, MG, Dominguez, MG, Mocci, S, Wetterwald, A, Felix, R, Fleisch, H, Chisholm, O, Hofstetter, W, Pollard, JW, Stanley, ER, Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120 (1994), 1357–1372.
18. [18] Clifford, AB, Elnaggar, AM, Robison, RA, O'Neill, K, Investigating the role of macrophages in tumor formation using a MaFIA mouse model. Oncol Rep 30 (2013), 890–896.
19. [19] Schwertfeger, KL, Xian, W, Kaplan, AM, Burnett, SH, Cohen, DA, Rosen, JM, A critical role for the inflammatory response in a mouse model of preneoplastic progression. Cancer Res 66 (2006), 5676–5685.
20. [20] Lal, S, Lacroix, M, Tofilon, P, Fuller, GN, Sawaya, R, Lang, FF, An implantable guide-screw system for brain tumor studies in small animals. J Neurosurg 92 (2000), 326–333.
21. [21] Attia, MA, Weiss, DW, Immunology of spontaneous mammary carcinomas in mice. V. Acquired tumor resistance and enhancement in strain A mice infected with mammary tumor virus. Cancer Res 26 (1966), 1787–1800.
22. [22] Lee, OH, Fueyo, J, Xu, J, Yung, WK, Lemoine, MG, Lang, FF, Bekele, BN, Zhou, X, Alonso, MA, Aldape, KD, et al. Sustained angiopoietin-2 expression disrupts vessel formation and inhibits glioma growth. Neoplasia 8 (2006), 419–428.
23. [23] Leten, C, Struys, T, Dresselaers, T, Himmelreich, U, In vivo and ex vivo assessment of the blood brain barrier integrity in different glioblastoma animal models. J Neurooncol 119 (2014), 297–306.
24. [24] Morris, SM Jr., Kepka-Lenhart, D, Chen, LC, Differential regulation of arginases and inducible nitric oxide synthase in murine macrophage cells. Am J Physiol 275 (1998), E740–E747.
25. [25] Sica, A, Larghi, P, Mancino, A, Rubino, L, Porta, C, Totaro, MG, Rimoldi, M, Biswas, SK, Allavena, P, Mantovani, A, Macrophage polarization in tumour progression. Semin Cancer Biol 18 (2008), 349–355.
26. [26] Sindrilaru, A, Peters, T, Wieschalka, S, Baican, C, Baican, A, Peter, H, Hainzl, A, Schatz, S, Qi, Y, Schlecht, A, et al. An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J Clin Invest 121 (2011), 985–997.
27. [27] Ries, CH, Cannarile, MA, Hoves, S, Benz, J, Wartha, K, Runza, V, Rey-Giraud, F, Pradel, LP, Feuerhake, F, Klaman, I, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 25 (2014), 846–859.
28. [28] Burnett, SH, Beus, BJ, Avdiushko, R, Qualls, J, Kaplan, AM, Cohen, DA, Development of peritoneal adhesions in macrophage depleted mice. J Surg Res 131 (2006), 296–301.
29. [29] Maes, W, Deroose, C, Reumers, V, Krylyshkina, O, Gijsbers, R, Baekelandt, V, Ceuppens, J, Debyser, Z, Van Gool, SW, In vivo bioluminescence imaging in an experimental mouse model for dendritic cell based immunotherapy against malignant glioma. J Neurooncol 91 (2009), 127–139.
30. [30] Szatmari, T, Lumniczky, K, Desaknai, S, Trajcevski, S, Hidvegi, EJ, Hamada, H, Safrany, G, Detailed characterization of the mouse glioma 261 tumor model for experimental glioblastoma therapy. Cancer Sci 97 (2006), 546–553.
31. [31] Zagzag, D, Miller, DC, Chiriboga, L, Yee, H, Newcomb, EW, Green fluorescent protein immunohistochemistry as a novel experimental tool for the detection of glioma cell invasion in vivo. Brain Pathol 13 (2003), 34–37.
32. [32] Gabrusiewicz, K, Ellert-Miklaszewska, A, Lipko, M, Sielska, M, Frankowska, M, Kaminska, B, Characteristics of the alternative phenotype of microglia/macrophages and its modulation in experimental gliomas. PLoS One, 6, 2011, e23902.
33. [33] Lawrence, T, Natoli, G, Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 11 (2011), 750–761.
34. [34] Sica, A, Mantovani, A, Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122 (2012), 787–795.
35. + T cells. Oncoimmunology, 2, 2013, e26968.
36. [36] 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 19 (2013), 1264–1272.