The PDGF-BB-SOX7 axis-modulated IL-33 in pericytes and stromal cells promotes metastasis through tumour-associated macrophages

Nature Communications

Volumn 7, Issue , 2016, Pages

  Yang, Yunlong ^a   Andersson, Patrik ^a   Hosaka, Kayoko ^a   Zhang, Yin ^a   Cao, Renhai ^a   Iwamoto, Hideki ^a   Yang, Xiaojuan ^a   Nakamura, Masaki ^a   Wang, Jian ^a   Zhuang, Rujie ^b   Morikawa, Hiromasa ^a   Xue, Yuan ^a,c   Braun, Harald ^d,e   Beyaert, Rudi ^d,e   Samani, Nilesh ^f   Nakae, Susumu ^g   Hams, Emily ^h   Dissing, Steen ⁱ   Fallon, Padraic G ^h   Langer, Robert ^c   Cao, Yihai ^a,f,j   more..

^a KAROLINSKA INSTITUTE   (Sweden)

^b TCM   (China)

^c Massachusetts Institute of Technology   (United States)

^d GHENT UNIVERSITY   (Belgium)

^e DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^f UNIVERSITY OF LEICESTER   (United Kingdom)

^g UNIVERSITY OF TOKYO   (Japan)

^h TRINITY COLLEGE DUBLIN   (Ireland)

ⁱ UNIVERSITY OF COPENHAGEN   (Denmark)

^j LINKÖPING UNIVERSITY   (Sweden)

more..

Author keywords

[No Author keywords available]

Indexed keywords

IMATINIB; INTERLEUKIN 33; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN; SOLUBLE ST2 PROTEIN; TRANSCRIPTION FACTOR SOX7; UNCLASSIFIED DRUG; BECAPLERMIN; PLATELET DERIVED GROWTH FACTOR B; SOX7 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

CANCER; CELLS AND CELL COMPONENTS; EXPERIMENTAL STUDY; GENE; GENETIC ANALYSIS; RODENT; TUMOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; GAIN OF FUNCTION MUTATION; GENE DELETION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; METASTASIS; MOUSE; NONHUMAN; PERICYTE; PROTEIN EXPRESSION; SQUAMOUS CELL CARCINOMA; STROMA CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR XENOGRAFT; UPREGULATION; ANIMAL; C57BL MOUSE; GENETICS; MACROPHAGE; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR CELL LINE;

MUS;

ANIMALS; CELL LINE, TUMOR; FEMALE; HUMANS; INTERLEUKIN-33; MACROPHAGES; MICE; MICE, INBRED C57BL; NEOPLASM METASTASIS; NEOPLASMS; PERICYTES; PROTO-ONCOGENE PROTEINS C-SIS; SOXF TRANSCRIPTION FACTORS; STROMAL CELLS;

EID: 84967184780     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11385     Document Type: Article

References (53)

1. Joyce, J. A., Pollard, J. W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252 (2009).
2. Langley, R. R., Fidler, I. J. Tumor cell-organ microenvironment interactions in the pathogenesis of cancer metastasis. Endocr. Rev. 28, 297-321 (2007).
3. Heldin, C. H., Westermark, B. Platelet-derived growth factor and autocrine mechanisms of oncogenic processes. Crit. Rev. Oncog. 2, 109-124 (1991).
4. Heinrich, M. C. et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299, 708-710 (2003).
5. Cao, Y. Multifarious functions of PDGFs and PDGFRs in tumor growth and metastasis. Trends Mol. Med. 19, 460-473 (2013).
6. Hellstrom, M. et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 153, 543-553 (2001).
7. Andrae, J., Gallini, R., Betsholtz, C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22, 1276-1312 (2008).
8. Hanahan, D., Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
9. Grivennikov, S. I., Greten, F. R., Karin, M. Immunity, inflammation, and cancer. Cell 140, 883-899 (2010).
10. Mantovani, A., Allavena, P., Sica, A., Balkwill, F. Cancer-related inflammation. Nature 454, 436-444 (2008).
11. Coussens, L. M., Werb, Z. Inflammation and cancer. Nature 420, 860-867 (2002).
12. Schmitz, J. et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23, 479-490 (2005).
13. Dinarello, C. A. An IL-1 family member requires caspase-1 processing and signals through the ST2 receptor. Immunity 23, 461-462 (2005).
14. Schiering, C. et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 513, 564-568 (2014).
15. Bonilla, W. V. et al. The alarmin interleukin-33 drives protective antiviral CD8(\+) T cell responses. Science 335, 984-989 (2012).
16. Jovanovic, I. P. et al. Interleukin-33/ST2 axis promotes breast cancer growth and metastases by facilitating intratumoral accumulation of immunosuppressive and innate lymphoid cells. Int. J. Cancer 134, 1669-1682 (2014).
17. Druker, B. J. et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 344, 1031-1037 (2001).
18. Gao, J. et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal. 6, pl1 (2013).
19. Uhlik, M. T. et al. Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat. Cell Biol. 5, 1104-1110 (2003).
20. Pleschka, S. et al. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat. Cell Biol. 3, 301-305 (2001).
21. Ito, K. et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 12, 446-451 (2006).
22. Dai, C. et al. Loss of tumor suppressor NF1 activates HSF1 to promote carcinogenesis. J. Clin. Invest. 122, 3742-3754 (2012).
23. Townsend, M. J., Fallon, P. G., Matthews, D. J., Jolin, H. E., McKenzie, A. N. T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J. Exp. Med. 191, 1069-1076 (2000).
24. Qian, B. Z. et al. CCL2 recruits inflammatory monocytes to facilitate breasttumour metastasis. Nature 475, 222-225 (2011).
25. Ji, H. et al. TNFR1 mediates TNF-alpha-induced tumour lymphangiogenesis and metastasis by modulating VEGF-C-VEGFR3 signalling. Nat. Commun. 5, 4944 (2014).
26. Rouhi, P. et al. Hypoxia-induced metastasis model in embryonic zebrafish. Nat. Protoc. 5, 1911-1918 (2010).
27. Lee, S. L. et al. Hypoxia-induced pathological angiogenesis mediates tumor cell dissemination, invasion, and metastasis in a zebrafish tumor model. Proc. Natl Acad. Sci. USA 106, 19485-19490 (2009).
28. Wang, J. et al. Novel mechanism of macrophage-mediated metastasis revealed in a zebrafish model of tumor development. Cancer Res. 75, 306-315 (2015).
29. Lawson, N. D., Weinstein, B. M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318 (2002).
30. Dahl Ejby, J. L. et al. Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish. Proc. Natl Acad. Sci. USA 106, 18408-18413 (2009).
31. Guabiraba, R. et al. IL-33 targeting attenuates intestinal mucositis and enhances effective tumor chemotherapy in mice. Mucosal Immunol. 7, 1079-1093 (2014).
32. Oboki, K. et al. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc. Natl Acad. Sci. USA 107, 18581-18586 (2010).
33. Bardeesy, N., DePinho, R. A. Pancreatic cancer biology and genetics. Nat. Rev. Cancer 2, 897-909 (2002).
34. Heldin, C. H., Westermark, B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79, 1283-1316 (1999).
35. Saito, S. et al. Ligand-independent trans-activation of the platelet-derived growth factor receptor by reactive oxygen species requires protein kinase C-delta and c-Src. J. Biol. Chem. 277, 44695-44700 (2002).
36. Herrlich, A. et al. Ligand-independent activation of platelet-derived growth factor receptor is a necessary intermediate in lysophosphatidic, acid-stimulated mitogenic activity in L cells. Proc. Natl Acad. Sci. USA 95, 8985-8990 (1998).
37. Drummond-Barbosa, D. A., Vaillancourt, R. R., Kazlauskas, A., DiMaio, D. Ligand-independent activation of the platelet-derived growth factor beta receptor: requirements for bovine papillomavirus E5-induced mitogenic signaling. Mol. Cell. Biol. 15, 2570-2581 (1995).
38. Warde-Farley, D. et al. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 38 Web Server issue W214-W220 (2010).
39. Lewis, C. E., Pollard, J. W. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 66, 605-612 (2006).
40. Cooke, V. G. et al. Pericyte depletion results in hypoxia-associated epithelial-tomesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell 21, 66-81 (2012).
41. Armulik, A., Genove, G., Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215 (2011).
42. Xian, X. et al. Pericytes limit tumor cell metastasis. J. Clin. Invest. 116, 642-651 (2006).
43. Carriere, V. et al. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl Acad. Sci. USA 104, 282-287 (2007).
44. Pollard, J. W. Tumour-educated macrophages promote tumour progression and metastasis. Nat. Rev. Cancer 4, 71-78 (2004).
45. Gao, K. et al. Transgenic expression of IL-33 activates CD8(\+) T cells and NK cells and inhibits tumor growth and metastasis in mice. Cancer Lett. 335, 463-471 (2013).
46. Gao, X. et al. Tumoral expression of IL-33 inhibits tumor growth and modifies the tumor microenvironment through CD8\+ T and NK cells. J. Immunol. 194, 438-445 (2015).
47. Villarreal, D. O. et al. Alarmin IL-33 acts as an immunoadjuvant to enhance antigen-specific tumor immunity. Cancer Res. 74, 1789-1800 (2014).
48. Xue, Y. et al. PDGF-BB modulates hematopoiesis and tumor angiogenesis by inducing erythropoietin production in stromal cells. Nat. Med. 18, 100-110 (2012).
49. Costa, G. et al. SOX7 regulates the expression of VE-cadherin in the haemogenic endothelium at the onset of haematopoietic development. Development 139, 1587-1598 (2012).
50. Cao, R. et al. Suppression of angiogenesis and tumor growth by the inhibitor K1-5 generated by plasmin-mediated proteolysis. Proc. Natl Acad. Sci. USA 96, 5728-5733 (1999).
51. Honek, J. et al. Modulation of age-related insulin sensitivity by VEGFdependent vascular plasticity in adipose tissues. Proc. Natl Acad. Sci. USA 111, 14906-14911 (2014).
52. Yang, X. et al. Vascular endothelial growth factor-dependent spatiotemporal dual roles of placental growth factor in modulation of angiogenesis and tumor growth. Proc. Natl Acad. Sci. USA 110, 13932-13937 (2013).
53. Hosaka, K. et al. Tumour PDGF-BB expression levels determine dual effects of anti-PDGF drugs on vascular remodelling and metastasis. Nat. Commun. 4, 2129 (2013).