Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth

Nature Cell Biology

Volumn 17, Issue 2, 2015, Pages 170-182

  Zhou, Wenchao ^a   Ke, Susan Q ^a   Huang, Zhi ^a   Flavahan, William ^a   Fang, Xiaoguang ^a   Paul, Jeremy ^a   Wu, Ling ^a   Sloan, Andrew E ^b   McLendon, Roger E ^c   Li, Xiaoxia ^a   Rich, Jeremy N ^a   Bao, Shideng ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR RUNX2; VITRONECTIN RECEPTOR; CELL ADHESION MOLECULE; CHEMOTACTIC FACTOR; POSTN PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER STEM CELL; CELL DENSITY; CELL MIGRATION; CONTROLLED STUDY; FEMALE; GLIOBLASTOMA; GLIOMA STEM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SURVIVAL RATE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR XENOGRAFT; ANIMAL; BLOOD; BRAIN TUMOR; C57BL MOUSE; CELL COUNT; CELL PROLIFERATION; DRUG SCREENING; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; LUMINESCENCE; MACROPHAGE; METABOLISM; MONOCYTE; PATHOLOGY; SECRETION (PROCESS); SURVIVAL; TUMOR CELL LINE;

MUS;

ANIMALS; BRAIN NEOPLASMS; CELL ADHESION MOLECULES; CELL COUNT; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOTACTIC FACTORS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; GLIOBLASTOMA; HUMANS; INTEGRIN ALPHAVBETA3; LUMINESCENT MEASUREMENTS; MACROPHAGES; MICE, INBRED C57BL; MONOCYTES; NEOPLASTIC STEM CELLS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84923068676     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3090     Document Type: Article

References (64)

1. Deorah, S., Lynch, C. F., Sibenaller, Z. A. & Ryken, T. C. Trends in brain cancer incidence and survival in the United States: Surveillance, Epidemiology, and End Results Program, 1973 to 2001. Neurosurg. Focus 20, E1 (2006).
2. DeAngelis, L. M. Brain tumors. N. Engl. J. Med. 344, 114-123 (2001).
3. Hao, C. et al. Cytokine and cytokine receptor mRNA expression in human glioblastomas: Evidence of Th1, Th2 and Th3 cytokine dysregulation. Acta Neuropathol. 103, 171-178 (2002).
4. Abou-Ghazal, M. et al. The incidence, correlation with tumor-infiltrating inflammation, and prognosis of phosphorylated STAT3 expression in human gliomas. Clin. Cancer Res. 14, 8228-8235 (2008).
5. Morford, L. A., Dix, A. R., Brooks, W. H. & Roszman, T. L. Apoptotic elimination of peripheral T lymphocytes in patients with primary intracranial tumors. J. Neurosurg. 91, 935-946 (1999).
6. Hirano, H., Tanioka, K., Yokoyama, S., Akiyama, S. & Kuratsu, J. Angiogenic effect of thymidine phosphorylase on macrophages in glioblastoma multiforme. J. Neurosurg. 95, 89-95 (2001).
7. Kanamori, M., Kawaguchi, T., Berger, M. S. & Pieper, R. O. Intracranial microenvironment reveals independent opposing functions of host-V-3 expression on glioma growth and angiogenesis. J. Biol. Chem. 281, 37256-37264 (2006).
8. Samaras, V. et al. Application of the ELISPOT method for comparative analysis of interleukin (IL)-6 and IL-10 secretion in peripheral blood of patients with astroglial tumors. Mol. Cell. Biochem. 304, 343-351 (2007).
9. Mineharu, Y. et al. Engineering the brain tumor microenvironment enhances the efficacy of dendritic cell vaccination: Implications for clinical trial design. Clin. Cancer Res. 17, 4705-4718 (2011).
10. Pellegatta, S. et al. Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res. 66, 10247-10252 (2006).
11. Graf, M. R., Prins, R. M., Hawkins, W. T. & Merchant, R. E. Irradiated tumor cell vaccine for treatment of an established glioma. I. Successful treatment with combined radiotherapy and cellular vaccination. Cancer Immunol. Immunother. 51, 179-189 (2002).
12. Sielska, M. et al. Distinct roles of CSF family cytokines in macrophage infiltration and activation in glioma progression and injury response. J. Pathol. 230, 310-321 (2013).
13. Staudt, N. D. et al. Myeloid cell receptor LRP1/CD91 regulates monocyte recruitment and angiogenesis in tumors. Cancer Res. 73, 3902-3912 (2013).
14. Pucci, F. et al. A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 114, 901-914 (2009).
15. Komohara, Y., Ohnishi, K., Kuratsu, J. & Takeya, M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J. Pathol. 216, 15-24 (2008).
16. Ling, E. A. & Wong, W. C. The origin and nature of ramified and amoeboid microglia: A historical review and current concepts. Glia 7, 9-18 (1993).
17. Deininger, M. H., Seid, K., Engel, S., Meyermann, R. & Schluesener, H. J. Allograft inflammatory factor-1 defines a distinct subset of infiltrating macrophages/microglial cells in rat and human gliomas. Acta Neuropathol. 100, 673-680 (2000).
18. Akiyama, H. & McGeer, P. L. Brain microglia constitutively express-2 integrins. J. Neuroimmunol. 30, 81-93 (1990).
19. Guvenc, H. et al. Impairment of glioma stem cell survival and growth by a novel inhibitor for Survivin-Ran protein complex. Clin. Cancer Res. 19, 631-642 (2013).
20. Tran, C. T. et al. Differential expression of MHC class II molecules by microglia and neoplastic astroglia: Relevance for the escape of astrocytoma cells from immune surveillance. Neuropathol. Appl. Neurobiol. 24, 293-301 (1998).
21. Ludwig, H. C. et al. Expression of nitric oxide synthase isozymes (NOS I-III) by immunohistochemistry and DNA in situ hybridization. Correlation with macrophage presence, vascular endothelial growth factor (VEGF) and oedema volumetric data in 220 glioblastomas. Anticancer Res. 20, 299-304 (2000).
22. Mizutani, M. et al. The fractalkine receptor but not CCR2 is present on microglia from embryonic development throughout adulthood. J. Immunol. 188, 29-36 (2012).
23. Ginestier, C. et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1, 555-567 (2007).
24. Singh, S. K. et al. Identification of human brain tumour initiating cells. Nature 432, 396-401 (2004).
25. Barker, N. et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608-611 (2009).
26. Bao, S. et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760 (2006).
27. Cheng, L. et al. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 153, 139-152 (2013).
28. Calabrese, C. et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11, 69-82 (2007).
29. Du, R. et al. HIF1-induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 13, 206-220 (2008).
30. Li, Z. et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15, 501-513 (2009).
31. Lathia, J. D., Heddleston, J. M., Venere, M. & Rich, J. N. Deadly teamwork: Neural cancer stem cells and the tumor microenvironment. Cell Stem Cell 8, 482-485 (2011).
32. Yang, I., Han, S. J., Sughrue, M. E., Tihan, T. & Parsa, A. T. Immune cell infiltrate differences in pilocytic astrocytoma and glioblastoma: Evidence of distinct immunological microenvironments that reflect tumor biology. J. Neurosurg. 115, 505-511 (2011).
33. Xing, F. et al. Hypoxia-induced Jagged2 promotes breast cancer metastasis and selfrenewal of cancer stem-like cells. Oncogene 30, 4075-4086 (2011).
34. Auffinger, B. et al. Conversion of differentiated cancer cells into cancer stem-like cells in a glioblastoma model after primary chemotherapy. Cell Death Differ. 21, 1119-1131 (2014).
35. Deininger, M. H., Pater, S., Strik, H. & Meyermann, R. Macrophage/microglial cell subpopulations in glioblastoma multiforme relapses are differentially altered by radiochemotherapy. J. Neurooncol. 55, 141-147 (2001).
36. Bao, S. et al. Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5, 329-339 (2004).
37. Baril, P. et al. Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxia-induced cell death: Role of the-4 integrin and the PI3k pathway. Oncogene 26, 2082-2094 (2007).
38. Malanchi, I. et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481, 85-89 (2012).
39. Michaylira, C. Z. et al. Periostin, a cell adhesion molecule, facilitates invasion in the tumor microenvironment and annotates a novel tumor-invasive signature in esophageal cancer. Cancer Res. 70, 5281-5292 (2010).
40. Koronyo-Hamaoui, M. et al. Attenuation of AD-like neuropathology by harnessing peripheral immune cells: Local elevation of IL-10 and MMP-9. J. Neurochem. 111, 1409-1424 (2009).
41. Jin, X., Ishii, H., Bai, Z., Itokazu, T. & Yamashita, T. Temporal changes in cell marker expression and cellular infiltration in a controlled cortical impact model in adult male C57BL/6 mice. PLoS ONE 7, e41892 (2012).
42. Saederup, N. et al. Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS ONE 5, e13693 (2010).
43. Movahedi, K. et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 70, 5728-5739 (2010).
44. Qian, B. Z. & Pollard, J. W. Macrophage diversity enhances tumor progression and metastasis. Cell 141, 39-51 (2010).
45. Sica, A. & Mantovani, A. Macrophage plasticity and polarization: In vivo veritas. J. Clin. Invest. 122, 787-795 (2012).
46. Yu, J. L. & Rak, J. W. Host microenvironment in breast cancer development: Inflammatory and immune cells in tumour angiogenesis and arteriogenesis. Breast Cancer Res. 5, 83-88 (2003).
47. Condeelis, J. & Pollard, J. W. Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell 124, 263-266 (2006).
48. Sica, A., Schioppa, T., Mantovani, A. & Allavena, P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: Potential targets of anti-cancer therapy. Eur. J. Cancer 42, 717-727 (2006).
49. Sharda, D. R. et al. Regulation of macrophage arginase expression and tumor growth by the Ron receptor tyrosine kinase. J. Immunol. 187, 2181-2192 (2011).
50. Arranz, A. et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc. Natl Acad. Sci. USA 109, 9517-9522 (2012).
51. Rolny, C. et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19, 31-44 (2011).
52. Wang, H. et al. Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation. J. Clin. Invest. 116, 2105-2114 (2006).
53. Gillan, L. et al. Periostin secreted by epithelial ovarian carcinoma is a ligand for-(V)-(3) and-(V)-(5) integrins and promotes cell motility. Cancer Res. 62, 5358-5364 (2002).
54. Butcher, J. T., Norris, R. A., Hoffman, S., Mjaatvedt, C. H. & Markwald, R. R. Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev. Biol. 302, 256-266 (2007).
55. Grkovich, A., Johnson, C. A., Buczynski, M. W. & Dennis, E. A. Lipopolysaccharideinduced cyclooxygenase-2 expression in human U937 macrophages is phosphatidic acid phosphohydrolase-1-dependent. J. Biol. Chem. 281, 32978-32987 (2006).
56. Shrivastav, A. et al. Requirement of N-myristoyltransferase 1 in the development of monocytic lineage. J. Immunol. 180, 1019-1028 (2008).
57. Stupp, R. et al. Phase I/IIa study of cilengitide and temozolomide with concomitant radiotherapy followed by cilengitide and temozolomide maintenance therapy in patients with newly diagnosed glioblastoma. J. Clin. Oncol. 28, 2712-2718 (2010).
58. 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. 23, 549-555 (2002).
59. Kim, D. W. et al. High tumour islet macrophage infiltration correlates with improved patient survival but not with EGFR mutations, gene copy number or protein expression in resected non-small cell lung cancer. Br. J. Cancer 98, 1118-1124 (2008).
60. Popivanova, B. K. et al. Blockade of a chemokine, CCL2, reduces chronic colitisassociated carcinogenesis in mice. Cancer Res. 69, 7884-7892 (2009).
61. Qian, B. Z. et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475, 222-225 (2011).
62. Pyonteck, S. M. et al. Deficiency of the macrophage growth factor CSF-1 disrupts pancreatic neuroendocrine tumor development. Oncogene 31, 1459-1467 (2012).
63. Spear, P., Barber, A., Rynda-Apple, A. & Sentman, C. L. Chimeric antigen receptor T cells shape myeloid cell function within the tumor microenvironment through IFN-and GM-CSF. J. Immunol. 188, 6389-6398 (2012).
64. Germano, G. et al. Role of macrophage targeting in the antitumor activity of trabectedin. Cancer Cell 23, 249-262 (2013).