No effect of NGAL/lipocalin-2 on aggressiveness of cancer in the MMTV-PYMT/FVB/N mouse model for breast cancer

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Cramer, Elisabeth P ^a   Glenthøj, Andreas ^a   Häger, Mattias ^a   Juncker Jensen, Anna ^b   Engelholm, Lars H ^b   Santoni Rugiu, Eric ^a   Lund, Leif R ^c   Laerum, Ole D ^b,d   Cowland, Jack B ^a   Borregaard, Niels ^a  

^a Rigshospitalet   (Denmark)

^b FINSEN LABORATORY   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRATE DEHYDROGENASE; LIPOCALIN 2RECEPTOR; MEGALIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; RECEPTOR; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; VIRUS MIDDLE T ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BREAST CANCER; BREAST CARCINOGENESIS; CONTROLLED STUDY; CROSS BREEDING; DISEASE MODEL; FEMALE; HISTOPATHOLOGY; MALE; METASTASIS POTENTIAL; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; MOUSE STRAIN; NONHUMAN; POLYOMA VIRUS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TUMOR VOLUME; WILD TYPE;

ACUTE-PHASE PROTEINS; ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GRANULOCYTES; HUMANS; IMMUNOHISTOCHEMISTRY; LIPOCALINS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-2; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; ONCOGENE PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, TRANSFERRIN;

EID: 84862703061     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039646     Document Type: Article

References (57)

1. Kjeldsen L, Bainton DF, Sengelov H, Borregaard N, (1994) Identification of neutrophil gelatinase-associated lipocalin as a novel matrix protein of specific granules in human neutrophils. Blood 83: 799-807.
2. Kjeldsen L, Johnsen AH, Sengelov H, Borregaard N, (1993) Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 268: 10425-10432.
3. Cancedda FD, Malpeli M, Gentili C, Di M, V, Bet P, et al. (1996) The developmentally regulated avian Ch21 lipocalin is an extracellular fatty acid-binding protein. J Biol Chem 271: 20163-20169.
4. Stoesz SP, Gould MN, (1995) Overexpression of neu-related lipocalin (NRL) in neu-initiated but not ras or chemically initiated rat mammary carcinomas. Oncogene 11: 2233-2241.
5. Flower DR, North AC, Attwood TK, (1991) Mouse oncogene protein 24p3 is a member of the lipocalin protein family. Biochem Biophys Res Commun 180: 69-74.
6. Beynon RJ, Hurst JL, (2003) Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochem Soc Trans 31: 142-146.
7. Holmes MA, Paulsene W, Jide X, Ratledge C, Strong RK, (2005) Siderocalin (Lcn 2) also binds carboxymycobactins, potentially defending against mycobacterial infections through iron sequestration. Structure 13: 29-41.
8. Cowland JB, Sorensen OE, Sehested M, Borregaard N, (2003) Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J Immunol 171: 6630-6639.
9. Karlsen JR, Borregaard N, Cowland JB, (2010) Induction of neutrophil gelatinase-associated lipocalin expression by co-stimulation with interleukin-17 and tumor necrosis factor-alpha is controlled by IkappaB-zeta but neither by C/EBP-beta nor C/EBP-delta. J Biol Chem 285: 14088-14100.
10. Mallbris L, O'Brien KP, Hulthen A, Sandstedt B, Cowland JB, et al. (2002) Neutrophil gelatinase-associated lipocalin is a marker for dysregulated keratinocyte differentiation in human skin. Exp Dermatol 11: 584-591.
11. Nielsen BS, Borregaard N, Bundgaard JR, Timshel S, Sehested M, et al. (1996) Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel diseases. Gut 38: 414-420.
12. Friedl A, Stoesz SP, Buckley P, Gould MN, (1999) Neutrophil gelatinase-associated lipocalin in normal and neoplastic human tissues. Cell type-specific pattern of expression. Histochem J 31: 433-441.
13. Stoesz SP, Friedl A, Haag JD, Lindstrom MJ, Clark GM, et al. (1998) Heterogeneous expression of the lipocalin NGAL in primary breast cancers. Int J Cancer 79: 565-572.
14. Mishra J, Mori K, Ma Q, Kelly C, Yang J, et al. (2004) Amelioration of ischemic acute renal injury by neutrophil gelatinase-associated lipocalin. J Am Soc Nephrol 15: 3073-3082.
15. Mishra J, Ma Q, Prada A, Mitsnefes M, Zahedi K, et al. (2003) Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol 14: 2534-2543.
16. Mishra J, Dent C, Tarabishi R, Mitsnefes MM, Ma Q, et al. (2005) Neutrophil gelatinase-associated lipocalin (NGAL) as a biomarker for acute renal injury after cardiac surgery. Lancet 365: 1231-1238.
17. Devarajan P, (2010) Review: neutrophil gelatinase-associated lipocalin: a troponin-like biomarker for human acute kidney injury. Nephrology (Carlton) 15: 419-428.
18. Goetz DH, Willie ST, Armen RS, Bratt T, Borregaard N, et al. (2000) Ligand preference inferred from the structure of neutrophil gelatinase associated lipocalin. Biochemistry 39: 1935-1941.
19. Goetz DH, Holmes MA, Borregaard N, Bluhm ME, Raymond KN, et al. (2002) The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 10: 1033-1043.
20. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, et al. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432: 917-921.
21. Berger T, Togawa A, Duncan GS, Elia AJ, You-Ten A, et al. (2006) Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc Natl Acad Sci U S A 103: 1834-1839.
22. Wu H, Santoni-Rugiu E, Ralfkiaer E, Porse BT, Moser C, et al. (2010) Lipocalin 2 is protective against E. coli pneumonia. Respir Res 11: 96.
23. Chan YR, Liu JS, Pociask DA, Zheng M, Mietzner TA, et al. (2009) Lipocalin 2 is required for pulmonary host defense against Klebsiella infection. J Immunol 182: 4947-4956.
24. Johnson EE, Srikanth CV, Sandgren A, Harrington L, Trebicka E, et al. (2010) Siderocalin inhibits the intracellular replication of Mycobacterium tuberculosis in macrophages. FEMS Immunol Med Microbiol 58: 138-145.
25. Saiga H, Nishimura J, Kuwata H, Okuyama M, Matsumoto S, et al. (2008) Lipocalin 2-dependent inhibition of mycobacterial growth in alveolar epithelium. J Immunol 181: 8521-8527.
26. Devireddy LR, Teodoro JG, Richard FA, Green MR, (2001) Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation. Science 293: 829-834.
27. Devireddy LR, Gazin C, Zhu X, Green MR, (2005) A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 123: 1293-1305.
28. Devireddy LR, Hart DO, Goetz DH, Green MR, (2010) A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell 141: 1006-1017.
29. Bao G, Clifton M, Hoette TM, Mori K, Deng SX, et al. (2010) Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex. Nat Chem Biol 6: 602-609.
30. Klausen P, Niemann CU, Cowland JB, Krabbe K, Borregaard N, (2005) On mouse and man: neutrophil gelatinase associated lipocalin is not involved in apoptosis or acute response. Eur J Haematol 75: 332-340.
31. Bauer M, Eickhoff JC, Gould MN, Mundhenke C, Maass N, et al. (2008) Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 108: 389-397.
32. Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, et al. (2009) Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci U S A 106: 3913-3918.
33. Kubben FJ, Sier CF, Hawinkels LJ, Tschesche H, van DW, et al. (2007) Clinical evidence for a protective role of lipocalin-2 against MMP-9 autodegradation and the impact for gastric cancer. Eur J Cancer 43: 1869-1876.
34. Tschesche H, Zolzer V, Triebel S, Bartsch S, (2001) The human neutrophil lipocalin supports the allosteric activation of matrix metalloproteinases. Eur J Biochem 268: 1918-1928.
35. Sevenich L, Schurigt U, Sachse K, Gajda M, Werner F, et al. (2010) Synergistic antitumor effects of combined cathepsin B and cathepsin Z deficiencies on breast cancer progression and metastasis in mice. Proc Natl Acad Sci U S A 107: 2497-2502.
36. Sevenich L, Werner F, Gajda M, Schurigt U, Sieber C, et al. (2011) Transgenic expression of human cathepsin B promotes progression and metastasis of polyoma-middle-T-induced breast cancer in mice. Oncogene 30: 54-64.
37. Vasiljeva O, Korovin M, Gajda M, Brodoefel H, Bojic L, et al. (2008) Reduced tumour cell proliferation and delayed development of high-grade mammary carcinomas in cathepsin B-deficient mice. Oncogene 27: 4191-4199.
38. Berger T, Cheung CC, Elia AJ, Mak TW, (2010) Disruption of the Lcn2 gene in mice suppresses primary mammary tumor formation but does not decrease lung metastasis. Proc Natl Acad Sci U S A 107: 2995-3000.
39. Leng X, Ding T, Lin H, Wang Y, Hu L, et al. (2009) Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 69: 8579-8584.
40. Euhus DM, Hudd C, LaRegina MC, Johnson FE, (1986) Tumor measurement in the nude mouse. J Surg Oncol 31: 229-234.
41. Juncker-Jensen A, Romer J, Pennington CJ, Lund LR, Almholt K, (2009) Spontaneous metastasis in matrix metalloproteinase 3-deficient mice. Mol Carcinog 48: 618-625.
42. Nielsen BS, Lund LR, Christensen IJ, Johnsen M, Usher PA, et al. (2001) A precise and efficient stereological method for determining murine lung metastasis volumes. Am J Pathol 158: 1997-2003.
43. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, et al. (2003) Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 163: 2113-2126.
44. Almholt K, Juncker-Jensen A, Laerum OD, Dano K, Johnsen M, et al. (2008) Metastasis is strongly reduced by the matrix metalloproteinase inhibitor Galardin in the MMTV-PymT transgenic breast cancer model. Mol Cancer Ther 7: 2758-2767.
45. Borregaard N, Heiple JM, Simons ER, Clark RA, (1983) Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation. J Cell Biol 97: 52-61.
46. Kjeldsen L, Bjerrum OW, Askaa J, Borregaard N, (1992) Subcellular localization and release of human neutrophil gelatinase, confirming the existence of separate gelatinase-containing granules. Biochem J 287 (Pt 2): 603-610.
47. Kjeldsen L, Koch C, Arnljots K, Borregaard N, (1996) Characterization of two ELISAs for NGAL, a newly described lipocalin in human neutrophils. J Immunol Methods 198: 155-164.
48. Mazzoni A, Mannello F, Tay FR, Tonti GA, Papa S, et al. (2007) Zymographic analysis and characterization of MMP-2 and-9 forms in human sound dentin. J Dent Res 86: 436-440.
49. Lifsted T, Le VT, Williams M, Muller W, Klein-Szanto A, et al. (1998) Identification of inbred mouse strains harboring genetic modifiers of mammary tumor age of onset and metastatic progression. Int J Cancer 77: 640-644.
50. Guy CT, Cardiff RD, Muller WJ, (1992) Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 12: 954-961.
51. Hvidberg V, Jacobsen C, Strong RK, Cowland JB, Moestrup SK, et al. (2005) The endocytic receptor megalin binds the iron transporting neutrophil-gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett 579: 773-777.
52. Liu Q, Nilsen-Hamilton M, (1995) Identification of a new acute phase protein. J Biol Chem 270: 22565-22570.
53. Davie SA, Maglione JE, Manner CK, Young D, Cardiff RD, et al. (2007) Effects of FVB/NJ and C57Bl/6J strain backgrounds on mammary tumor phenotype in inducible nitric oxide synthase deficient mice. Transgenic Res 16: 193-201.
54. Martin MD, Carter KJ, Jean-Philippe SR, Chang M, Mobashery S, et al. (2008) Effect of ablation or inhibition of stromal matrix metalloproteinase-9 on lung metastasis in a breast cancer model is dependent on genetic background. Cancer Res 68: 6251-6259.
55. Almholt K, Green KA, Juncker-Jensen A, Nielsen BS, Lund LR, et al. (2007) Extracellular proteolysis in transgenic mouse models of breast cancer. J Mammary Gland Biol Neoplasia 12: 83-97.
56. Almholt K, Lund LR, Rygaard J, Nielsen BS, Dano K, et al. (2005) Reduced metastasis of transgenic mammary cancer in urokinase-deficient mice. Int J Cancer 113: 525-532.
57. Fernandez CA, Yan L, Louis G, Yang J, Kutok JL, et al. (2005) The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 11: 5390-5395.