Tumour-associated macrophages correlate with poor prognosis in myxoid liposarcoma and promote cell motility and invasion via the HB-EGF-EGFR-PI3K/Akt pathways

British Journal of Cancer

Volumn 112, Issue 3, 2015, Pages 547-555

  Nabeshima, A ^a   Matsumoto, Y ^a   Fukushi, J ^a   Iura, K ^a   Matsunobu, T ^a   Endo, M ^a   Fujiwara, T ^a   Iida, K ^a   Fujiwara, Y ^a   Hatano, M ^a   Yokoyama, N ^a   Fukushima, S ^a   Oda, Y ^a   Iwamoto, Y ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

EGF receptor; heparin binding EGF like growth factor; myxoid liposarcoma; PI3K Akt; tumour associated macrophages

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ARTICLE; CANCER PROGNOSIS; CELL INFILTRATION; CELL INVASION; CELL MOTILITY; DISEASE ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MACROPHAGE INFILTRATION; MAJOR CLINICAL STUDY; MYXOSARCOMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; WESTERN BLOTTING; WOUND HEALING;

EID: 84964284448     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.637     Document Type: Article

References (32)

1. Aman P, Ron D, Mandahl N, Fioretos T, Heim S, Arheden K, Willen H Rydholm A, Mitelman F (1992) Rearrangement of the transcription factor gene CHOP in myxoid liposarcomas with t(12;16)(q13;p11). Genes Chromosomes Cancer 5(4): 278-285.
2. Antonescu CR, Ladanyi M (2013) Myxoid liposarcoma. In World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of Soft Tissue and Bone, Fletcher CD, Bridge JA, Hogendoorn PC Mertens F (eds)pp 39-41. IARC Press: Lyon.
3. Antonescu CR, Tschernyavsky SJ, Decuseara R, Leung DH, Woodruff JM Brennan MF, Bridge JA, Neff JR, Goldblum JR, Ladanyi M (2001) Prognostic impact of P53 status, TLS-CHOP fusion transcript structure and histological grade in myxoid liposarcoma: a molecular and clinicopathologic study of 82 cases. Clin Cancer Res 7(12): 3977-3987.
4. Asano N, Susa M, Hosaka S, Nakayama R, Kobayashi E, Takeuchi K, Horiuchi K, Suzuki Y, Anazawa U, Mukai M, Toyama Y, Yabe H, Morioka H (2012) Metastatic patterns of myxoid/round cell liposarcoma: a review of a 25-year experience. Sarcoma 2012: 345161.
5. Baay M, Brouwer A, Pauwels P, Peeters M, Lardon F (2011) Tumor cells and tumor-associated macrophages: secreted proteins as potential targets for therapy. Clin Dev Immunol 2011: 565187.
6. Buddingh EP, Kuijjer ML, Duim RA, Burger H, Agelopoulos K, Myklebost O Serra M, Mertens F, Hogendoorn PC, Lankester AC, Cleton-Jansen AM (2011) Tumor-infiltrating macrophages are associated with metastasis suppression in high-grade osteosarcoma: a rationale for treatment with macrophage activating agents. Clin Cancer Res 17(8): 2110-2119.
7. Carr MW, Roth SJ, Luther E, Rose SS, Springer TA (1994) Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc Natl Acad Sci USA 91(9): 3652-3656.
8. Cheng H, Dodge J, Mehl E, Liu S, Poulin N, van de Rijn M, Nielsen TO (2009) Validation of immature adipogenic status and identification of prognostic biomarkers in myxoid liposarcoma using tissue microarrays. Hum Pathol 40(9): 1244-1251.
9. Condeelis J, Pollard JW (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124(2): 263-266.
10. Demicco EG, Torres KE, Ghadimi MP, Colombo C, Bolshakov S, Hoffman A Peng T, Bovee JV,WangWL, Lev D, Lazar AJ (2012) Involvement of the PI3K/ Akt pathway in myxoid/round cell liposarcoma. Mod Pathol 25(2): 212-221.
11. Engelman JA (2009) Targeting PI3K signalling in cancer: opportunities challenges and limitations. Nat Rev Cancer 9(8): 550-562.
12. Fujiwara-Okada Y, Matsumoto Y, Fukushi J, Setsu N, Matsuura S, Kamura S Fujiwara T, Iida K, Hatano M, Nabeshima A, Yamada H, Ono M, Oda Y Iwamoto Y (2013) Y-box binding protein-1 regulates cell proliferation and is associated with clinical outcomes of osteosarcoma. Br J Cancer 108(4): 836-847.
13. Fujiwara T, Fukushi J, Yamamoto S, Matsumoto Y, Setsu N, Oda Y, Yamada H Okada S, Watari K, Ono M, Kuwano M, Kamura S, Iida K, Okada Y Koga M, Iwamoto Y (2011) Macrophage infiltration predicts a poor prognosis for human ewing sarcoma. Am J Pathol 179(3): 1157-1170.
14. Goerdt S, Orfanos CE (1999) Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10(2): 137-142.
15. Haniball J, Sumathi VP, Kindblom LG, Abudu A, Carter SR, Tillman RM Jeys L, Spooner D, Peake D, Grimer RJ (2011) Prognostic factors and metastatic patterns in primary myxoid/round-cell liposarcoma. Sarcoma 2011: 538085.
16. Harimaya K, Tanaka K, Matsumoto Y, Sato H, Matsuda S, Iwamoto Y (2000) Antioxidants inhibit TNFalpha-induced motility and invasion of human osteosarcoma cells: possible involvement of NFkappaB activation. Clin Exp Metastasis 18(2): 121-129.
17. Hoffmann AC, Danenberg KD, Taubert H, Danenberg PV, Wuerl P (2009) A three-gene signature for outcome in soft tissue sarcoma. Clin Cancer Res 15(16): 5191-5198.
18. Hubbard SR, Miller WT (2007) Receptor tyrosine kinases: mechanisms of activation and signaling. Curr Opin Cell Biol 19(2): 117-123.
19. Iida K, Fukushi J, Matsumoto Y, Oda Y, Takahashi Y, Fujiwara T Fujiwara-Okada Y, Hatano M, Nabashima A, Kamura S, Iwamoto Y (2013) miR-125b develops chemoresistance in Ewing sarcoma/primitive neuroectodermal tumor. Cancer Cell Int 13(1): 21.
20. Kamura S, Matsumoto Y, Fukushi JI, Fujiwara T, Iida K, Okada Y, Iwamoto Y (2010) Basic fibroblast growth factor in the bone microenvironment enhances cell motility and invasion of Ewings sarcoma family of tumours by activating the FGFR1-PI3K-Rac1 pathway. Br J Cancer 103(3): 370-381.
21. Komohara Y, Jinushi M, Takeya M (2013) Clinical significance of macrophage heterogeneity in human malignant tumors. Cancer Sci 105(1): 1-8.
22. Lee CH, Espinosa I, Vrijaldenhoven S, Subramanian S, Montgomery KD Zhu S, Marinelli RJ, Peterse JL, Poulin N, Nielsen TO, West RB, Gilks CB van de Rijn M (2008) Prognostic significance of macrophage infiltration in leiomyosarcomas. Clin Cancer Res 14(5): 1423-1430.
23. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL (1996) Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 56(20): 4625-4629.
24. Matsumoto Y, Tanaka K, Hirata G, Hanada M, Matsuda S, Shuto T Iwamoto Y (2002) Possible involvement of the vascular endothelial growth factor-Flt-1-focal adhesion kinase pathway in chemotaxis and the cell proliferation of osteoclast precursor cells in arthritic joints. J Immunol 168(11): 5824-5831.
25. Miyamoto S, Yagi H, Yotsumoto F, Kawarabayashi T, Mekada E (2006) Heparin-binding epidermal growth factor-like growth factor as a novel targeting molecule for cancer therapy. Cancer Sci 97(5): 341-347.
26. Nanba D, Higashiyama S (2004) Dual intracellular signaling by proteolytic cleavage of membrane-anchored heparin-binding EGF-like growth factor. Cytokine Growth Factor Rev 15(1): 13-19.
27. Negri T, Virdis E, Brich S, Bozzi F, Tamborini E, Tarantino E Jocolle G, Cassinelli G, Grosso F, Sanfilippo R, Casalini P Greco A, Pierotti MA, Pilotti S (2010) Functional mapping of receptor tyrosine kinases in myxoid liposarcoma. Clin Cancer Res 16(14): 3581-3593.
28. Oda Y, Yamamoto H, Takahira T, Kobayashi C, Kawaguchi K Tateishi N, Nozuka Y, Tamiya S, Tanaka K, Matsuda S, Yokoyama R Iwamoto Y, Tsuneyoshi M (2005) Frequent alteration of p16(INK4a)/ p14(ARF) and p53 pathways in the round cell component of myxoid/ round cell liposarcoma: p53 gene alterations and reduced p14(ARF) expression both correlate with poor prognosis. J Pathol 207(4): 410-421.
29. Pietras K, Ostman A (2010) Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res 316(8): 1324-1331.
30. Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141(1): 39-51.
31. Rigo A, Gottardi M, Zamo A, Mauri P, Bonifacio M, Krampera M, Damiani E Pizzolo G, Vinante F (2010) Macrophages may promote cancer growth via a GM-CSF/HB-EGF paracrine loop that is enhanced by CXCL12. Mol Cancer 9: 273.
32. Vlaicu P, Mertins P, Mayr T, Widschwendter P, Ataseven B, Hogel B Eiermann W, Knyazev P, Ullrich A (2013) Monocytes/macrophages support mammary tumor invasivity by co-secreting lineage-specific EGFR ligands and a STAT3 activator. BMC Cancer 13: 197.