Tumour stroma-derived lipocalin-2 promotes breast cancer metastasis

Journal of Pathology

Volumn 239, Issue 3, 2016, Pages 274-285

  Ören, Bilge ^a   Urosevic, Jelena ^b   Mertens, Christina ^a   Mora, Javier ^a,d   Guiu, Marc ^b   Gomis, Roger R ^b,c   Weigert, Andreas ^a   Schmid, Tobias ^a   Grein, Stephan ^a   Brüne, Bernhard ^a   Jung, Michaela ^a  

^a GOETHE UNIVERSITY   (Germany)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

breast cancer; EMT; Lipocalin 2; macrophage; metastasis; tumour stroma

Indexed keywords

KI 67 ANTIGEN; NERVE CELL ADHESION MOLECULE; NEUTRALIZING ANTIBODY; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MACROPHAGE; MCF 7 CELL LINE; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; STROMA; SUPERNATANT; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; TUMOR GROWTH; TUMOR MODEL; TUMOR SPHEROID; TUMOR STROMA; TUMOR XENOGRAFT; WILD TYPE;

EID: 84976272253     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4724     Document Type: Article

References (32)

1. Kjeldsen L, Johnsen AH, Sengelov H, et al. Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 1993; 268: 10425–10432.
2. Virzì GM, Clementi A, de Cal M, et al. Genomics and biological activity of neutrophil gelatinase-associated lipocalin in several clinical settings. Blood Purif 2013; 35: 139–143.
3. Flo TH, Smith KD, Sato S, et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004; 432: 917–921.
4. Sola A, Weigert A, Jung M, et al. Sphingosine-1-phosphate signalling induces the production of Lcn-2 by macrophages to promote kidney regeneration. J Pathol 2011; 225: 597–608.
5. Srinivasan G, Aitken JD, Zhang B, et al. Lipocalin 2 deficiency dysregulates iron homeostasis and exacerbates endotoxin-induced sepsis. J Immunol 2012; 189: 1911–1919.
6. Rodvold JJ, Mahadevan NR, Zanetti M. Lipocalin 2 in cancer: when good immunity goes bad. Cancer Lett 2012; 316: 132–138.
7. Leng X, Wu Y, Arlinghaus RB. Relationships of lipocalin 2 with breast tumorigenesis and metastasis. J Cell Physiol 2011; 226: 309–314.
8. Yang J, Moses MA. Lipocalin 2: A multifaceted modulator of human cancer. Cell Cycle 2009; 8: 2347–2352.
9. Yang J, Bielenberg DR, Rodig SJ, et al. Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 2009; 106: 3913–3918.
10. Chakraborty S, Kaur S, Guha S, et al. The multifaceted roles of neutrophil gelatinase associated lipocalin (NGAL) in inflammation and cancer. Biochim Biophys Acta 2012; 1826: 129–169.
11. Shi H, Gu Y, Yang J, et al. Lipocalin 2 promotes lung metastasis of murine breast cancer cells. J Exp Clin Cancer Res 2008; 27: 83.
12. Yan L, Borregaard N, Kjeldsen L, et al. The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 2001; 276: 37258–37265.
13. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metast Rev 2006; 25: 9–34.
14. Kubben FJGM, Sier CFM, Hawinkels LJAC, et al. Clinical evidence for a protective role of lipocalin-2 against MMP-9 autodegradation and the impact for gastric cancer. Eur J Cancer 2007; 43: 1869–1876.
15. Gheorgheosu D, Jung M, Oren B, et al. Betulinic acid suppresses NGAL-induced epithelial-to-mesenchymal transition in melanoma. Biol Chem 2013; 394: 773–781.
16. Leng X, Ding T, Lin H, et al. Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 2009; 69: 8579–8584.
17. Berger T, Cheung CC, Elia AJ, et al. Disruption of the Lcn2 gene in mice suppresses primary mammary tumor formation but does not decrease lung metastasis. Proc Natl Acad Sci USA 2010; 107: 2995–3000.
18. Cramer EP, Glenthoj A, Hager M, et al. No effect of NGAL/lipocalin-2 on aggressiveness of cancer in the MMTV-PyMT/FVB/N mouse model for breast cancer. PloS One 2012; 7: e39646.
19. Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013; 19: 1423–1437.
20. Jung M, Mertens C, Brüne B. Macrophage iron homeostasis and polarization in the context of cancer. Immunobiology 2015; 220: 295–304.
21. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010; 141: 39–51.
22. Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol 2009; 9: 259–270.
23. Rohan TE, Xue X, Lin H, et al. Tumor microenvironment of metastasis and risk of distant metastasis of breast cancer. J Natl Cancer Inst 2014; 106: dju136.
24. Jung M, Weigert A, Tausendschon M, et al. Interleukin-10-induced neutrophil gelatinase-associated lipocalin production in macrophages with consequences for tumor growth. Mol Cell Biol 2012; 32: 3938–3948.
25. Jung M, Sola A, Hughes J, et al. Infusion of IL-10-expressing cells protects against renal ischemia through induction of lipocalin-2. Kidney Int 2012; 81: 969–982.
26. Minn AJ, Gupta GP, Siegel PM, et al. Genes that mediate breast cancer metastasis to lung. Nature 2005; 436: 518–524.
27. Werno C, Menrad H, Weigert A, et al. Knockout of HIF-1α in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses. Carcinogenesis 2010; 31: 1863–1872.
28. Shinriki S, Jono H, Ueda M, et al. Stromal expression of neutrophil gelatinase-associated lipocalin correlates with poor differentiation and adverse prognosis in oral squamous cell carcinoma. Histopathology 2014; 64: 356–364.
29. Zhou N, Zhang Y, Zhang X, et al. Exposure of tumor-associated macrophages to apoptotic MCF-7 cells promotes breast cancer growth and metastasis. Int J Mol Sci 2015; 16: 11966–11982.
30. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metast Rev 2009; 28: 15–33.
31. Hazan RB. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 2000; 148: 779–790.
32. Christiansen JJ, Rajasekaran AK. Reassessing epithelial-to-mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006; 66: 8319–8326.