Irradiation promotes an M2 macrophage phenotype in tumor hypoxia

Frontiers in Oncology

Volumn 2 AUG, Issue , 2012, Pages

  Chiang, Chi Shiun ^a   Fu, Sheng Yung ^a,b   Wang, Shu Chi ^a   Yu, Ching Fang ^a   Chen, Fang Hsin ^a   Li, Chi Min ^a   Hong, Ji Hong ^b  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Radiation; Tumor microenvironment; Tumor associated macrophages

Indexed keywords

ANTIGEN; ARGINASE 1; CD11B ANTIGEN; CD68 ANTIGEN; GELATINASE A; GRANULOCYTE DIFFERENTIATION ANTIGEN 1; STROMAL CELL DERIVED FACTOR 1ALPHA; SUNITINIB; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; HYPOXIA; IMMUNOHISTOCHEMISTRY; INFLAMMATORY CELL; IRRADIATION; LEUKOCYTE AGGREGATION; MALE; MICROARRAY ANALYSIS; MOUSE; NEOPLASM; NONHUMAN; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH;

EID: 84875024405     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2012.00089     Document Type: Article

References (55)

1. Ahn, G. O., and Brown, J. M. (2008). Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell 13, 193-205.
2. Ahn, G. O., Tseng, D., Liao, C. H., Dorie, M. J., Czechowicz, A., and Brown, J. M. (2010). Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc. Natl. Acad. Sci. U.S.A. 107, 8363-8368.
3. Alizadeh, D., Zhang, L., Hwang, J., Schluep, T., and Badie, B. (2010). Tumor-associated macrophages are predominant carriers of cyclodextrin-based nanoparticles into gliomas. Nanomedicine 6, 382-390.
4. Benoit, D. S., Henry, S. M., Shubin, A. D., Hoffman, A. S., and Stayton, P. S. (2010). pH-responsive polymeric sirna carriers sensitize multidrug resistant ovarian cancer cells to doxorubicin via knockdown of polo-like kinase 1. Mol. Pharm. 7, 442-455.
5. Bingle, L., Brown, N. J., and Lewis, C. E. (2002). The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 196, 254-265.
6. Burke, B., Giannoudis, A., Corke, K. P., Gill, D., Wells, M., Ziegler-Heitbrock, L., and Lewis, C. E. (2003). Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am. J. Pathol. 163, 1233-1243.
7. Burke, B., Tang, N., Corke, K. P., Tazzyman, D., Ameri, K., Wells, M., and Lewis, C. E. (2002). Expression of HIF-1alpha by human macrophages: implications for the use of macrophages in hypoxia-regulated cancer gene therapy. J. Pathol. 196, 204-212.
8. Chen, F. H., Chiang, C. S., Wang, C. C., Fu, S. Y., Tsai, C. S., Jung, S. M., Wen, C. J., Lee, C. C., and Hong, J. H. (2011). Vasculatures in tumors growing from preirradiated tissues: formed by vasculogenesis and resistant to radiation and antiangiogenic therapy. Int. J. Radiat. Oncol. Biol. Phys. 80, 1512-1521.
9. Chen, F. H., Chiang, C. S., Wang, C. C., Tsai, C. S., Jung, S. M., Lee, C. C., McBride, W. H., and Hong, J. H. (2009). Radiotherapy decreases vascular density and causes hypoxia with macrophage aggregation in TRAMP-C1 prostate tumors. Clin. Cancer Res. 15, 1721-1729.
10. Chiang, C. S., Chen, F. H., Hong, J. H., Jiang, P. S., Huang, H. L., Wang, C. C., and McBride, W. H. (2008). Functional phenotype of macrophages depends on assay procedures. Int. Immunol. 20, 215-222.
11. Chiu, H. C., Hsiue, G. H., Lee, Y. P., and Huang, L. W. (1999). Synthesis and characterization of pH-sensitive dextran hydrogels as a potential colon-specific drug delivery system. J. Biomater. Sci. Polym. Ed. 10, 591-608.
12. Corzo, C. A., Condamine, T., Lu, L., Cotter, M. J., Youn, J. I., Cheng, P., Cho, H. I., Celis, E., Quiceno, D. G., Padhya, T., McCaffrey, T. V., McCaffrey, J. C., and Gabrilovich, D. I. (2010). HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207, 2439-2453.
13. Crowther, M., Brown, N. J., Bishop, E. T., and Lewis, C. E. (2001). Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J. Leukoc. Biol. 70, 478-490.
14. Degrossoli, A., and Giorgio, S. (2007). Functional alterations in macrophages after hypoxia selection. Exp. Biol. Med. (Maywood) 232, 88-95.
15. Denardo, D. G., Brennan, D. J., Rexhepaj, E., Ruffell, B., Shiao, S. L., Madden, S. F., Gallagher, W. M., Wadhwani, N., Keil, S. D., Junaid, S. A., Rugo, H. S., Hwang, E. S., Jirstrom, K., West, B. L., and Coussens, L. M. (2011). Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov. 1, 54-67.
16. Dirkx, A. E., Oude Egbrink, M. G., Wagstaff, J., and Griffioen, A. W. (2006). Monocyte/macrophage infiltration in tumors: modulators of angiogenesis. J. Leukoc. Biol. 80, 1183-1196.
17. Foster, B. A., Gingrich, J. R., Kwon, E. D., Madias, C., and Greenberg, N. M. (1997). Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res. 57, 3325-3330.
18. Gazitt, Y., and Akay, C. (2004). Mobilization of myeloma cells involves SDF-1/CXCR4 signaling and downregulation of VLA-4. Stem Cells 22, 65-73.
19. Hanada, T., Nakagawa, M., Emoto, A., Nomura, T., Nasu, N., and Nomura, Y. (2000). Prognostic value of tumor-associated macrophage count in human bladder cancer. Int. J. Urol. 7, 263-269.
20. Ide, T., Kitajima, Y., Miyoshi, A., Ohtsuka, T., Mitsuno, M., Ohtaka, K., Koga, Y., and Miyazaki, K. (2006). Tumor-stromal cell interaction under hypoxia increases the invasiveness of pancreatic cancer cells through the hepatocyte growth factor/c-Met pathway. Int. J. Cancer 119, 2750-2759.
21. Jiang, H., De Ridder, M., Verovski, V. N., Sonveaux, P., Jordan, B. F., Law, K., Monsaert, C., Van Den Berge, D. L., Verellen, D., Feron, O., Gallez, B., and Storme, G. A. (2010). Activated macrophages as a novel determinant of tumor cell radioresponse: the role of nitric oxide-mediated inhibition of cellular respiration and oxygen sparing. Int. J. Radiat. Oncol. Biol. Phys. 76, 1520-1527.
22. Kang, J. C., Chen, J. S., Lee, C. H., Chang, J. J., and Shieh, Y. S. (2010). Intratumoral macrophage counts correlate with tumor progression in colorectal cancer. J. Surg. Oncol. 102, 242-248.
23. Kioi, M., Vogel, H., Schultz, G., Hoffman, R. M., Harsh, G. R., and Brown, J. M. (2010). Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 120, 694-705.
24. Leek, R. D., Landers, R. J., Harris, A. L., and Lewis, C. E. (1999). Necrosis correlates with high vascular density and focal macrophage infiltration in invasive carcinoma of the breast. Br. J. Cancer 79, 991-995.
25. Leek, R. D., Lewis, C. E., Whitehouse, R., Greenall, M., Clarke, J., and Harris, A. L. (1996). Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 56, 4625-4629.
26. Lewis, C., and Murdoch, C. (2005). Macrophage responses to hypoxia: implications for tumor progression and anti-cancer therapies. Am. J. Pathol. 167, 627-635.
27. Lewis, C. E., and Pollard, J. W. (2006). Distinct role of macrophages in different tumor microenvironments. Cancer Res. 66, 605-612.
28. Lewis, J. S., Landers, R. J., Underwood, J. C., Harris, A. L., and Lewis, C. E. (2000). Expression of vascular endothelial growth factor by macrophages is up-regulated in poorly vascularized areas of breast carcinomas. J. Pathol. 192, 150-158.
29. Lewis, J. S., Lee, J. A., Underwood, J. C., Harris, A. L., and Lewis, C. E. (1999). Macrophage responses to hypoxia: relevance to disease mechanisms. J. Leukoc. Biol. 66, 889-900.
30. Li, F., Sonveaux, P., Rabbani, Z. N., Liu, S., Yan, B., Huang, Q., Vujaskovic, Z., Dewhirst, M. W., and Li, C. Y. (2007). Regulation of HIF-1alpha stability through S-nitrosylation. Mol. Cell 26, 63-74.
31. Lin, E. Y., Li, J. F., Gnatovskiy, L., Deng, Y., Zhu, L., Grzesik, D. A., Qian, H., Xue, X. N., and Pollard, J. W. (2006). Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66, 11238-11246.
32. Mantovani, A., Ming, W. J., Balotta, C., Abdeljalil, B., and Bottazzi, B. (1986). Origin and regulation of tumor-associated macrophages: the role of tumor-derived chemotactic factor. Biochim. Biophys. Acta 865, 59-67.
33. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., and Sica, A. (2002). Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549-555.
34. Murdoch, C., Giannoudis, A., and Lewis, C. E. (2004). Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood 104, 2224-2234.
35. Murdoch, C., and Lewis, C. E. (2005). Macrophage migration and gene expression in response to tumor hypoxia. Int. J. Cancer 117, 701-708.
36. Murdoch, C., Muthana, M., and Lewis, C. E. (2005). Hypoxia regulates macrophage functions in inflammation. J. Immunol. 175, 6257-6263.
37. Muthana, M., Giannoudis, A., Scott, S. D., Fang, H. Y., Coffelt, S. B., Morrow, F. J., Murdoch, C., Burton, J., Cross, N., Burke, B., Mistry, R., Hamdy, F., Brown, N. J., Georgopoulos, L., Hoskin, P., Essand, M., Lewis, C. E., and Maitland, N. J. (2011). Use of macrophages to target therapeutic adenovirus to human prostate tumors. Cancer Res. 71, 1805-1815.
38. Newcomb, E. W., Lukyanov, Y., Kawashima, N., Alonso-Basanta, M., Wang, S. C., Liu, M., Jure-Kunkel, M., Zagzag, D., Demaria, S., and Formenti, S. C. (2010). Radiotherapy enhances antitumor effect of anti-CD137 therapy in a mouse Glioma model. Radiat. Res. 173, 426-432.
39. Nishie, A., Ono, M., Shono, T., Fukushi, J., Otsubo, M., Onoue, H., Ito, Y., Inamura, T., Ikezaki, K., Fukui, M., Iwaki, T., and Kuwano, M. (1999). Macrophage infiltration and heme oxygenase-1 expression correlate with angiogenesis in human gliomas. Clin. Cancer Res. 5, 1107-1113.
40. Ohno, S., Inagawa, H., Dhar, D. K., Fujii, T., Ueda, S., Tachibana, M., Suzuki, N., Inoue, M., Soma, G., and Nagasue, N. (2003). The degree of macrophage infiltration into the cancer cell nest is a significant predictor of survival in gastric cancer patients. Anticancer Res. 23, 5015-5022.
41. Qian, B. Z., and Pollard, J. W. (2010). Macrophage diversity enhances tumor progression and metastasis. Cell 141, 39-51.
42. Rauh-Hain, J. A., and Penson, R. T. (2008). Potential benefit of Sunitinib in recurrent and refractory ovarian clear cell adenocarcinoma. Int. J. Gynecol. Cancer 18, 934-936.
43. Redente, E. F., Dwyer-Nield, L. D., Merrick, D. T., Raina, K., Agarwal, R., Pao, W., Rice, P. L., Shroyer, K. R., and Malkinson, A. M. (2010). Tumor progression stage and anatomical site regulate tumor-associated macrophage and bone marrow-derived monocyte polarization. Am. J. Pathol. 176, 2972-2985.
44. Robinson, M. A., Baumgardner, J. E., and Otto, C. M. (2011). Oxygen-dependent regulation of nitric oxide production by inducible nitric oxide synthase. Free Radic. Biol. Med. 51, 1952-1965.
45. Stout, R. D., Jiang, C., Matta, B., Tietzel, I., Watkins, S. K., and Suttles, J. (2005). Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J. Immunol. 175, 342-349.
46. Tabatabai, G., Frank, B., Mohle, R., Weller, M., and Wick, W. (2006). Irradiation and hypoxia promote homing of haematopoietic progenitor cells towards gliomas by TGF-beta-dependent HIF-1alpha-mediated induction of CXCL12. Brain 129, 2426-2435.
47. Tsai, C. S., Chen, F. H., Wang, C. C., Huang, H. L., Jung, S. M., Wu, C. J., Lee, C. C., McBride, W. H., Chiang, C. S., and Hong, J. H. (2007). Macrophages from irradiated tumors express higher levels of iNOS, arginase-I and COX-2, and promote tumor growth. Int. J. Radiat. Oncol. Biol. Phys. 68, 499-507.
48. Vicini, F. A., Kestin, L., Huang, R., and Martinez, A. (2003). Does local recurrence affect the rate of distant metastases and survival in patients with early-stage breast carcinoma treated with breast-conserving therapy? Cancer 97, 910-919.
49. Wang, S. C., Hong, J. H., Hsueh, C., and Chiang, C. S. (2012). Tumor-secreted SDF-1 promotes glioma invasiveness and TAM tropism toward hypoxia in a murine astrocytoma model. Lab. Invest. 92, 151-162.
50. Wang, T. H., Lee, Y. S., Chen, E. S., Kong, W. H., Chen, L. K., Hsueh, D. W., Wei, M. L., and Wang, H. S. (2004). Establishment of cDNA microarray analysis at the Genomic Medicine Research Core Laboratory (GMRCL) of Chang Gung Memorial Hospital. Chang Gung Med. J. 27, 243-260.
51. Weigert, A., and Brune, B. (2008). Nitric oxide, apoptosis and macrophage polarization during tumor progression. Nitric Oxide 19, 95-102.
52. Williams, J. L., Cartland, D., Hussain, A., and Egginton, S. (2006). A differential role for nitric oxide in two forms of physiological angiogenesis in mouse. J. Physiol. (Lond.) 570, 445-454.
53. Zagzag, D., Lukyanov, Y., Lan, L., Ali, M. A., Esencay, M., Mendez, O., Yee, H., Voura, E. B., and Newcomb, E. W. (2006). Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab. Invest. 86, 1221-1232.
54. Zhang, W., Zhu, X. D., Sun, H. C., Xiong, Y. Q., Zhuang, P. Y., Xu, H. X., Kong, L. Q., Wang, L., Wu, W. Z., and Tang, Z. Y. (2010). Depletion of tumor-associated macrophages enhances the effect of sorafenib in metastatic liver cancer models by antimetastatic and antiangiogenic effects. Clin. Cancer Res. 16, 3420-3430.
55. Zhou, J., Dehne, N., and Brune, B. (2009). Nitric oxide causes macrophage migration via the HIF-1-stimulated small GTPases Cdc42 and Rac1. Free Radic. Biol. Med. 47, 741-749.