Tumor-derived interleukin-1 promotes lymphangiogenesis and lymph node metastasis through M2-type macrophages

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Watari, Kosuke ^a   Shibata, Tomohiro ^a   Kawahara, Akihiko ^b   Sata, Ken Ichi ^a   Nabeshima, Hiroshi ^a   Shinoda, Ai ^a   Abe, Hideyuki ^b   Azuma, Koichi ^c   Murakami, Yuichi ^a,d   Izumi, Hiroto ^e   Takahashi, Takashi ^f   Kage, Masayoshi ^b   Kuwano, Michihiko ^a   Ono, Mayumi ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KURUME UNIVERSITY HOSPITAL   (Japan)

^c KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d ST MARY S HOSPITAL   (Japan)

^e UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^f NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; VASCULOTROPIN A; VASCULOTROPIN C; CHEMOKINE; COLLAGEN; DRUG COMBINATION; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; LAMININ; MATRIGEL; PROTEOGLYCAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INFLAMMATION; LUNG CANCER; LUNG CANCER CELL LINE; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; M2 TYPE MACROPHAGE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CELL PROLIFERATION; COCULTURE; DRUG COMBINATION; DRUG EFFECTS; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); NEUTROPHIL CHEMOTAXIS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOKINES; COCULTURE TECHNIQUES; COLLAGEN; DRUG COMBINATIONS; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; LAMININ; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; MACROPHAGES; MALE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEUTROPHIL INFILTRATION; PROTEOGLYCANS; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 84903398786     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099568     Document Type: Article

References (41)

1. Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86: 353-364. (Pubitemid 26272076)
2. Achen MG, McColl BK, Stacker SA (2005) Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7: 121-127. (Pubitemid 40248338)
3. Cao Y (2005) Opinion: Emerging mechanisms of tumour lymphangiogenesis and lymphatic metastasis. Nat Rev Cancer 5: 735-743.
4. Balkwill F, Mantovani A (2001) Inflammation and cancer: Back to Virchow? Lancet 357: 539-545. (Pubitemid 32173595)
5. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420: 860-867. (Pubitemid 36019639)
6. Ono M. (2008) Molecular links between tumor angiogenesis and inflammation: Inflammatory stimuli of macrophages and cancer cells as targets for therapeutic strategy. Cancer Sci 99: 1501-1506.
7. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, et al. (2004) VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113: 1040-1050. (Pubitemid 38544126)
8. Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4: 71-78.
9. Costa C, Incio J, Soares R (2007) Angiogenesis and chronic inflammation: Cause or consequence? Angiogenesis 10: 149-166. (Pubitemid 47305203)
10. Sica A, Bronte V (2007) Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 117: 1155-1166. (Pubitemid 46718400)
11. Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141: 39-51.
12. Kuwano T, Nakao S, Yamamoto H, Tsuneyoshi M, Yamamoto T, et al. (2004) Cyclooxygenase 2 is a key enzyme for inflammatory cytokine-induced angiogenesis. FASEB J 18: 300-310. (Pubitemid 38186249)
13. Nakao S, Kuwano T, Tsutsumi-Miyahara C, Ueda S, Kimura YN, et al. (2005) Infiltration of COX-2-expressing macrophages is a prerequisite for IL-1 beta-induced neovascularization and tumor growth. J Clin Invest 115: 2979-2991. (Pubitemid 41567564)
14. Kimura YN, Watari K, Fotovati A, Hosoi F, Yasumoto K, et al. (2007) Inflammatory stimuli from macrophages and cancer cells synergistically promote tumor growth and angiogenesis. Cancer Sci 98: 2009-2018. (Pubitemid 350002210)
15. Watari K, Nakao S, Fotovati A, Basaki Y, Hosoi F, et al. (2008) Role of macrophages in inflammatory lymphangiogenesis: Enhanced production of vascular endothelial growth factor C and D through NF-kappaB activation. Biochem Biophys Res Commun 377: 826-831.
16. Koukourakis MI, Giatromanolaki A, Kakolyris S, O'Byrne KJ, Apostolikas N, et al. (1998) Different patterns of stromal and cancer cell thymidine phosphorylase reactivity in non-small-cell lung cancer: Impact on tumour neoangiogenesis and survival. Br J Cancer 77: 1696-1703. (Pubitemid 28230477)
17. Bingle L, Brown NJ, Lewis CE (2002) The role of tumour-associated macrophages in tumour progression: Implications for new anticancer therapies. J Pathol 196: 254-265. (Pubitemid 34189413)
18. Pollard JW (2009) Trophic macrophages in development and disease. Nat Rev Immunol 9: 259-270.
19. Kozaki K, Miyaishi O, Tsukamoto T, Tatematsu Y, Hida T, et al. (2000) Establishment and characterization of a human lung cancer cell line NCI-H460-LNM35 with consistent lymphogenous metastasis via both subcutaneous and orthotopic propagation. Cancer Res 60: 2535-2540. (Pubitemid 30262449)
20. Kozaki K, Koshikawa K, Tatematsu Y, Miyaishi O, Saito H, et al. (2001) Multi-faceted analyses of a highly metastatic human lung cancer cell line NCI-H460-LNM35 suggest mimicry of inflammatory cells in metastasis. Oncogene 20: 4228-4234. (Pubitemid 32762197)
21. He Y, Rajantie I, Pajusola K, Jeltsch M, Holopainen T, et al. (2005) Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res 65: 4739-4746. (Pubitemid 40740810)
22. He Y, Kozaki K, Karpanen T, Koshikawa K, Yla-Herttuala S, et al. (2002) Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst 94: 819-825. (Pubitemid 34705053)
23. Heckman CA, Holopainen T, Wirzenius M, Keskitalo S, Jeltsch M, et al. (2008) The tyrosine kinase inhibitor cediranib blocks ligand-induced vascular endothelial growth factor receptor-3 activity and lymphangiogenesis. Cancer Res 68: 4754-4762.
24. Holopainen T, Saharinen P, D'Amico G, Lampinen A, Eklund L, et al. (2012) Effects of angiopoietin-2-blocking antibody on endothelial cell-cell junctions and lung metastasis. J Natl Cancer Inst 104: 461-475.
25. Murakami Y, Watari K, Shibata T, Uba M, Ureshino H, et al. (2013) N-myc downstream-regulated gene 1 promotes tumor inflammatory angiogenesis through JNK activation and autocrine loop of interleukin-1α by human gastric cancer cells. J Biol Chem 288: 25025-25037.
26. Hiraoka K, Zenmyo M, Watari K, Iguchi H, Fotovati A, et al. (2008) Inhibition of bone and muscle metastases of lung cancer cells by a decrease in the number of monocytes/macrophages. Cancer Sci 99: 1595-1602.
27. Fujiwara T, Fukushi J, Yamamoto S, Matsumoto Y, Setsu N, et al. (2011) Macrophage infiltration predicts a poor prognosis for human ewing sarcoma. Am J Pathol 179: 1157-1170.
28. Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454: 436-444.
29. Apte RN, Dotan S, Elkabets M, White MR, Reich E, et al. (2006) The involvement of IL-1 in tumorigenesis, tumor invasiveness, metastasis and tumorhost interactions. Cancer Metastasis Rev 25: 387-408. (Pubitemid 44922357)
30. Apte RN, Voronov E (2008) Is interleukin-1 a good or bad 'guy' in tumor immunobiology and immunotherapy? Immunol Rev 222: 222-241. (Pubitemid 351430377)
31. Torisu H, Ono M, Kiryu H, Furue M, Ohmoto Y, et al. (2000) Macrophage infiltration correlates with tumor stage and angiogenesis in human malignant melanoma: Possible involvement of TNFalpha and IL-1alpha. Int J Cancer 85: 182-188. (Pubitemid 30023065)
32. Voronov E, Dotan S, Krelin Y, Song X, Elkabets M, et al. (2013) Unique Versus Redundant Functions of IL-1α and IL-1β in the Tumor Microenvironment. Front Immunol 4: Article 177.
33. Ling J, Kang Y, Zhao R, Xia Q, Lee DF, et al. (2012) KrasG12D-induced IKK2/β/NF-κB activation by IL-1α and p62 feedforward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell 21: 105-120.
34. Hagemann T, Lawrence T, McNeish I, Charles KA, Kulbe H, et al. (2008) "Reeducating" tumor-associated macrophages by targeting NF-kappaB. J Exp Med 205: 1261-1268. (Pubitemid 351831483)
35. Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, et al. (2001) Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20: 672-682. (Pubitemid 32167632)
36. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, et al. (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7: 192-198. (Pubitemid 32148486)
37. Kajita T, Ohta Y, Kimura K, Tamura M, Tanaka Y, et al. (2001) The expression of vascular endothelial growth factor C and its receptors in non-small cell lung cancer. Br J Cancer 85: 255-260. (Pubitemid 32695748)
38. Orlandini M, Oliviero S (2001) In fibroblasts Vegf-D expression is induced by cell-cell contact mediated by cadherin-11. J Biol Chem 276: 6576-6581.
39. Enholm B, Paavonen K, Ristimäki A, Kumar V, Gunji Y, et al. (1997) Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene 14: 2475-2483. (Pubitemid 27268166)
40. Ristimäki A, Narko K, Enholm B, Joukov V, Alitalo K (1998) Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J Biol Chem 273: 8413-8418. (Pubitemid 28168903)
41. Tsai PW, Shiah SG, Lin MT, Wu CW, Kuo ML (2003) Up-regulation of vascular endothelial growth factor C in breast cancer cells by heregulin-beta 1. A critical role of p38/nuclear factor-kappa B signaling pathway. J Biol Chem 278: 5750-5759.